A comparative analysis of vibrissa count and infraorbital foramen area in primates and other mammals

Journal of Human Evolution 58 (2010) 447e473

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A comparative analysis of vibrissa count and infraorbital foramen area in primates and other mammals Magdalena N. Muchlinski Department of Anatomy and Pathology, Marshall University e School of Medicine, 1542 Spring Valley Drive, Huntington, WV 25704, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Received 30 September 2008 Accepted 23 January 2010

Vibrissae are specialized sensory “hairs” that respond to mechanical stimuli. Sensory information from vibrissae is transmitted to the brain via the infraorbital nerve, which passes through the infraorbital foramen (IOF). Several analyses have documented that primates have smaller IOFs than non-primate mammals, and that haplorhines have smaller IOFs than strepsirrhines. These grade shifts in IOF area were attributed to differences in “vibrissa development.” Following earlier analyses, IOF area has been used to derive a general estimate of “whiskeredness” in extinct primates, and consequently, IOF area has been used in phylogenetic and paleoecological interpretations. Yet, the relationship between IOF area and vibrissa count has not been tested, and little is known about how IOF area and vibrissa counts vary among mammals. This study explores how relative IOF area and vibrissa count differ among 25 mammalian orders, and tests for a correlation between IOF area and vibrissa count. Results indicate that primates and dermopterans (Primatomorpha) have smaller IOFs than most non-primate mammals, but they do not have fewer vibrissae. In addition, strepsirrhines and haplorhines do not differ from one another in relative IOF area or vibrissa counts. Despite different patterns documented for IOF area and vibrissa count variation across mammals, results from this study do confirm that vibrissa count and IOF area are significantly and positively correlated (p < 0.0001). However, there is considerable scatter in the data, suggesting that vibrissa counts cannot be predicted from IOF area. There are three implications of these finding. First, IOF area reflects all mechanoreceptors in the maxillary region, not just vibrissae. Second, IOF area may be an informative feature in interpretations of the fossil record. Third, paleoecological interpretations based on vibrissae are not recommended. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Vibrissae Infraorbital foramen area Infraorbital nerve Euarchontan phylogeny Fossil record

Introduction Vibrissae are specialized sensory hairs that respond to mechanical stimuli such as tension, pressure, and displacement (Brecht et al., 1997; Marshall et al., 2006). All therian mammals, with a few exceptions (e.g., anteaters), have vibrissae (Cave, 1969; van Horn, 1970) that can be found throughout the external surface of the body where hair or fur is present (Lyne, 1959). Vibrissae are thicker than surrounding hairs, making them easily distinguishable from regular hair and fur. Like hair and fur, vibrissae reside in follicles, but the follicles penetrate deeper into the skin, forming a thickening around the shaft known as a rete ridge collar (Ebara et al., 2002). Recently, the term follicle-sinus complex was applied to the follicles of vibrissae to differentiate them from hair and fur follicles, which are associated with different sensory receptors (Rice, 1995). The specialized mechanoreceptors associated with vibrissae are Pacinian corpuscles, Merkel’s discs, and Ruffini corpuscles (Renehan and Munger, 1986; Munger and Ide, 1988; Halata, 1993; E-mail address: [email protected] 0047-2484/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2010.01.012

Dehnhardt et al., 1999; Ebara et al., 2002). These mechanoreceptors are housed within the follicle-sinus complex around the vibrissa shaft, so that even small displacements of the vibrissa will trigger a sensory response (Ebara et al., 2002). The best-studied vibrissae are the mystacial vibrissae (a.k.a., sinus hairs: Hill, 1960; Hofer, 1976), which are found on the maxillary region of the face. There are two types of mystacial vibrissae: macro- and micro-vibrissae. Macro-vibrissae are the long, laterally oriented hairs that are usually arranged in distinct organized rows on the muzzle. Micro-vibrissae are shorter, less organized, and confined to the area just above the upper lip (Fig. 1; Lyne, 1959; Brecht et al., 1997). Most previous studies have focused on macro-vibrissae, since they are considered to be of greater importance to mammalian environmental navigation (Brecht et al., 1997). However, recent work has called this assumption into question by suggesting that the macro-vibrissae appear to be critical for spatial tasks, while micro-vibrissae are involved in object recognition (Brecht et al., 1997). Variation in vibrissa length and number among species has been correlated to differences in diet, substrate preferences, and activity

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M.N. Muchlinski / Journal of Human Evolution 58 (2010) 447e473

have fewer and less pronounced vibrissae than most other mammals. He also proposed a “gradual failure [of vibrissae] in primates passing from the lower to the higher types” (Pocock, 1914: 912). Since Pocock’s research, similar trends in vibrissae reduction have been proposed for the two primate suborders (Jones, 1929; Hüber, 1930; Clark, 1959; Hershkovitz, 1977). Given the apparent trends in vibrissa count reduction in primates and suggested variation within the order, vibrissa count estimates could assist in addressing phylogenetic questions in fossil primates. Vibrissae and the infraorbital foramen

Fig. 1. A photograph of a strepsirrhine primate’s (Microcebus) muzzle. Macro-vibrissae are the laterally oriented hairs; the micro-vibrissae are the short hairs located along the upper lip. The rete ridge collar can be easily seen at the base of the right macrovibrissae.

pattern. For example, Pocock (1914) and Ahl (1987) demonstrated that arboreal animals have longer and more numerous macrovibrissae than terrestrial species. Because macro-vibrissae aid in spatial tasks, Ahl (1987) suggested that longer and more plentiful macro-vibrissae may be adaptive for navigating cluttered environments like the terminal branches of trees. Vincent (1913) and Kratochvil (1968) linked total macro-vibrissa count with activity pattern by documenting that nocturnal rodents have higher macrovibrissa counts than diurnal rodents. Because some nocturnal mammals are less dependent on vision than diurnal mammals, Kratochvil (1968) concluded that macro-vibrissae are of greater importance to nocturnal mammals for spatially detecting objects that are near the face. Experimental and observational studies also suggest that both macro- and micro-vibrissae aid in food acquisition (Ling, 1977; Leyhausen, 1979; Demble and Lewis, 1982; Dehnhardt and Kaminski, 1995; Schilling, 2000). Some researchers have concluded that macro-vibrissae aid in both the detection and capture of insects, and the amputation of these sensory hairs leads to greater kill latency times (Demble and Lewis, 1982; Anjum et al., 2006). On the other hand, Schilling’s (2000) work on the sensory organs of the mouse lemur (Microcebus) suggests that vibrissae (non-specific as to type) facilitate fruit selection because they assist in texture and shape discrimination. Although the conclusions regarding the ecological relevance of vibrissae differ among researchers, all agree that vibrissae increase an animal’s ability both to detect mechanical stimuli and assist in spatial and tactile object recognition tasks. Currently, we know very little about vibrissa variation among mammals, or how variation is influenced by an animal’s ecology. A better understanding of vibrissa variation and the development of methods by which to predict vibrissa differences may aid in paleoecological interpretations of the fossil record. Because vibrissa count varies significantly among mammalian orders (Pocock, 1914), this feature has been proposed to be an informative character for distinguishing mammals from one another at the ordinal, generic, and species levels (Frédéric, 1906; Pocock, 1914; Lyne, 1959; Montagna, 1967; van Horn, 1970; Marshall et al., 2006). A reduction in the number of vibrissae has been reported in Artiodactyla, Perissodactyla, and Xenarthra (Pocock, 1914; Cave, 1969). In 1914, Pocock reported that primates

The ability to approximate vibrissa counts in fossils is problematic because hair rarely preserves in the fossil record. Currently, only circumstantial evidence suggests that the size of the infraorbital foramen (IOF) can be used to predict vibrissa count in mammals. Variation in relative vibrissa count has been presented as an explanation for documented grade shifts in relative IOF area among mammals (Kay and Cartmill, 1977; Martin, 1999). Kay and Cartmill (1977) found that carnivores and “insectivores” (Afrosoricida, Soricomorpha, and Scandentia) have the largest IOFs of all mammals sampled, followed in decreasing size by marsupials, strepsirrhines, and haplorhines. They noted that “for the sampled marsupials, foramen size roughly reflects number and development of the mystacial vibrissae” (Kay and Cartmill, 1977: 42). Szalay (1981) also documents a similar pattern in IOF area reduction across mammals. Although Szalay (1981) never attributed IOF size variation to vibrissae, he did suggest that the documented variation in IOF area in mammals may be a result of phylogeny rather than function. For decades the IOF has been used in interpretations of the fossil record e yet, to date, the relationship between IOF area and vibrissa counts across mammals has never been systematically tested. The association between the IOF and vibrissae is based on an inferred relationship between the infraorbital nerve (ION) and vibrissae. The ION passes through the IOF on its way to the maxillary region, where it innervates the specialized mechanoreceptors around the shaft of both macro- and micro-vibrissae (Renehan and Munger, 1986; Munger and Ide, 1988; Halata, 1993; Dehnhardt et al., 1999; Ebara et al., 2002). Research on aquatic mammals and rodents suggests that maxillary mechanoreceptive sensitivity correlates with mechanoreceptor density (Dehnhardt and Kaminski, 1995; Nicolelis et al., 1997), and receptor density is expected to covary with total vibrissa count. Therefore, animals with a higher number of vibrissae should have a higher concentration of mechanoreceptors than animals with fewer vibrissae. Regions with higher receptor concentrations need more nerve fibers (and thus thicker nerves) to transmit sensory information (Wineski, 1983; Ebara et al., 2002). Recent anatomical research shows a strong correlation between IOF and ION cross-sectional area, where 80e90% of foramen area is explained by cross-sectional area of the ION (Muchlinski, 2008). Nerve cross-sectional area is a reliable measure of total nerve axon count (Jonas et al., 1992; Mackinnon and Dellon, 1995; Cull et al., 2003). The implication of these findings is that animals with larger IOFs (and therefore, larger IONs) would have more receptors and consequently, more vibrissae. Objectives The first objective of this study is to explore how relative IOF area varies among mammals. Specifically, this study will evaluate whether primates have smaller IOFs than other mammals and whether haplorhines have smaller IOFs than strepsirrhines. Based on previous research (Kay and Cartmill, 1977; Martin, 1999), I

M.N. Muchlinski / Journal of Human Evolution 58 (2010) 447e473

predict that these grade shifts will be observed. The second objective is to evaluate how vibrissa count differs among mammals and between primate suborders. For decades, it has been suggested that primates have fewer vibrissae than other mammals and that haplorhines have fewer vibrissae than strepsirrhines (Jones, 1929; Hüber, 1930; Clark, 1959; Hershkovitz, 1977). I predict that vibrissa count will distinguish all primates from non-primate mammals, and haplorhines from strepsirrhines. The third objective is to determine whether IOF area can be used to predict vibrissa count. Anecdotal reports of differences in vibrissa count in mammals suggest that vibrissa count will correlate with IOF area (Kay and Cartmill, 1977; Martin, 1999). If a strong predictive correlation exists between IOF area and vibrissa count, IOF area can be used to reconstruct vibrissa count in fossil primates, with implications for phylogenetic and paleoecological analyses of the fossil record. Materials and methods Sample The area of the IOF and number of mystacial vibrissae were quantified in a sample of 3488 osteological museum specimens (species n ¼ 527; Table 1) and 634 fluid-preserved cadavers (species n ¼ 238; Table 2). This sample includes representatives of eight metatherian orders and seventeen eutherian orders. All osteological measurements were made using adult skeletal material, and vibrissa counts were obtained from fluid-preserved cadavers. Both adult and sub-adult mammalian cadavers were used to obtain vibrissa counts because these counts do not differ with age post-adolescence (Lyne, 1959). Infraorbital foramen measurements The IOF is an irregularly-shaped foramen. To obtain an accurate measure of IOF cross-sectional area (IOF area), molds of the IOF were created, sectioned, photographed, and measured (in mm2) following protocols described in Muchlinski (2010). Mystacial vibrissa counts A dissection microscope was used to count macro- and microvibrissa on either the left or right side of each cadaver’s face. Macroand micro-vibrissae are distinct from one other in length and location, which allowed for an independent count of each vibrissa type (Fig. 1). In some instances, the rete ridge collar was observed, but the vibrissa was missing, presumably because it fell out peri- or post-mortem. In those instances, the rete ridge collar was counted and treated as a surrogate for an actual vibrissa. Vibrissae were counted on only half of the face to compare the count with one IOF area value. As the ION passes through the IOF, it only innervates vibrissae on the side of the face through which it passes. The median values for macro- and micro-vibrissa count were calculated for each species. Total vibrissa count values were calculated for each species by adding median macro- and micro-vibrissa counts together (Table 2). Size adjustment variables Both IOF area and all vibrissae counts correlate significantly with body mass (IOF area: r ¼ 0.84, p < 0.0001; macro-vibrissae: r ¼ 0.56, p < 0.0001; micro-vibrissae: r ¼ 0.61, p < 0.0001; total vibrissa count: r ¼ 0.57, p < 0.0001). Museum specimens are rarely associated with body mass data. In order to compare IOF area and vibrissa count across a wide range of body sizes, the two variables

449

need to be size-adjusted. Body mass is an approximation of body size, and the geometric mean of cranial shape correlates well with body mass (Mosimann, 1970; Jungers, 1985). Cranial length and maximum bizygomatic width were measured on all osteological specimens to calculate a geometric mean (GM) of cranial length and width as follows:

GM ¼

pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi cranial length  cranial width

Bizygomatic width is the linear distance between the most lateral points on the zygomatic arches. Maximum cranial length is the distance between prosthion and opisthocranion in the median sagittal plane. To test the relationship between GM and body mass, body mass data were compiled from the literature for a subset of this study’s sample (non-primate mammals: Silva and Downing, 1995; primates: Smith and Jungers, 1997). The subset included 53 primate species and 153 species from 10 non-primate mammalian orders (5 specimens per species). The GM values were highly correlated with body mass (BM) (Spearman’s r ¼ 0.97; p < 0.0001), and scale with slight negative allometry, but the confidence intervals (CI) include isometry (Reduced Major Axis [RMA]: r2 ¼ 0.97; ln GM ¼ 3.93 þ 0.29 ln BM; CI 0.29e0.33). GM scales with body mass similarly within orders as it does across all orders sampled. Given the high correlation coefficient and the scaling relationship between GM and body mass, GM can be used as a proxy for body mass. IOF area and all vibrissae variables scale isometrically with GM (RMA regression: ln IOF area ¼ 7.02 þ 2.02 ln GM, CI 1.94e3.22, r2 ¼ 0.84; ln macro-vibrissae ¼ 1.29 þ 1.11 ln GM, CI 0.96e1.28, r2 ¼ 0.50; ln micro-vibrissae ¼ 1.29 þ 1.09 ln GM, CI 0.95e1.26, r2 ¼ 0.50; ln total vibrissae ¼ 0.31 þ 1.03 ln GM, CI 0.91e1.16, r2 ¼ 0.50). Statistical analysis Infraorbital foramen area variation among mammals: To examine how IOF area varies across mammals, ln IOF area was regressed separately against ln GM for non-primate mammals and for primates, and an analysis of covariance (ANCOVA) was used to test for differences in IOF area (with GM as covariate). Next, ln IOF area was plotted against ln GM. Two rodent suborders (Hystricomorpha and Myomorpha) were excluded from this analysis, because these rodents have a portion of the masseter that passes through the IOF. The unique morphology of these rodents makes direct comparisons of relative IOF area between these suborders and all other mammals difficult. Similar analyses were run to test for differences between (1) primates and metatherian mammals, (2) primates and non-primate eutherian mammals, (3) Euarchonta and all other mammals, (4) Euarchontoglires and all other mammals, and (5) strepsirhines and haplorhines. All data examined using an ANCOVA met model assumptions (i.e., regression slopes were not significantly different). Only the results for differences in y-intercept will be presented. Significance was set at p < 0.05 for all ANCOVA pairwise comparisons. Residuals were calculated for the least squares regression of ln IOF area and ln GM. The relationship between the residual variation in IOF area and ln GM will hereafter be referred to as “relative” IOF area. For this analysis, the hystricomorphous and myomorphous rodents were once again removed from the sample. A Wilcoxon Rank Sum test was carried out to identify which mammalian orders differ significantly from primates in relative IOF area. Non-parametric test statistics were chosen because of the unequal ordinal sample sizes. A power and sample size analysis was run to test whether orders with few or one species could be compared with

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M.N. Muchlinski / Journal of Human Evolution 58 (2010) 447e473

Table 1 Infraorbital foramen area (IOF) and geometric mean (GM) of cranial length and width for 527 mammal species. n

IOF area Mean

Eutherian Afrosoricida Chrysochloridae Chlorotalpa leucorhina Chlorotalpa stuhlmanni Tenrecidae Echinops telfairi Geogale aurita Hemicentetes semispinosus Microgale talazaci Micropotamogale lamottei Potamogale velox Setifer setosus Tenrec ecaudatus Artiodactyla Antilocapridae Antilocapra americana Bovidae Addax nasomaculatus Aepyceros melampus Antilope cervicapra Bison bison Bubalus bubalis Capra sibirica Cephalophus leucogaster Connochaete taurinus Damaliscus lunatus Gazella bilkis Kobus vardonii Madoqua kirkii Nemorhaedus sumatraensis Oryx gazella Ourebia ourebi Ovibos moschatus Ovis ammon Pseudois nayaur Raphicerus campestris Redunca fulvorufula Rupicapra rupicapra Sigmoceros lichtensteinii Syncerus caffer Taurotragus oryx Bos taurus Artiodactyla Camelidae Camelus dromedarius Lama guanicoe Vicugna vicugna Giraffidae Giraffa camelopardalis Okapia johnstoni Hippopotamidae Hippopotamus amphibius Suidae Hylochoerus meinertzhageni Phacochoerus aethiopicus Sus barbatus Tayassuidae Pecari tajacu Tragulidae Tragulus kanchil Carnivora Canidae Canis lupus Canis simensis Cuon alpinus Lycaon pictus Otocyon megalotis Pseudalopex griseus Urocyon cinereoargenteus Vulpes vulpes

Min

GM Max

SD

Mean

Min

Max

SD

2 5

1.31 0.60

1.30 0.46

1.31 0.83

0.01 0.15

19.59 20.29

19.39 19.21

19.80 20.85

0.29 0.66

14 8 10 10 1 10 7 10

1.62 0.24 0.88 1.57 8.75 7.85 3.74 4.38

1.04 0.15 0.43 1.36 8.75 6.41 1.78 3.45

1.85 0.34 1.25 1.77 8.75 11.23 5.50 5.40

0.27 0.07 0.39 0.20

20.26 10.64 21.92 21.13 23.45 36.58 29.86 43.29

25.04 11.77 24.16 22.49 23.45 41.41 34.81 55.12

1.73 0.48 0.85 0.49

1.66 1.57 0.72

22.77 11.24 23.34 21.74 23.45 38.81 31.60 49.85

3

15.49

9.93

19.27

4.92

203.14

199.54

207.49

4.03

4 3 3 3 3 3 3 3 3 3 3 3 4 3 3 4 3 3 3 3 3 3 3 3 2

23.80 17.18 10.78 75.56 72.54 18.56 11.49 69.35 30.55 5.58 16.86 4.01 15.65 31.62 4.70 42.87 59.93 14.49 4.68 11.78 8.33 34.80 54.10 53.27 78.43

20.61 13.04 9.17 62.78 71.26 13.76 8.55 55.09 26.31 4.74 12.51 3.42 10.05 28.22 4.11 38.00 53.91 12.21 3.70 7.51 6.50 30.42 44.09 45.19 76.69

28.55 19.31 13.12 85.90 73.81 25.82 13.37 83.75 37.01 6.30 20.29 4.36 24.05 37.80 5.42 47.77 65.97 16.47 5.25 17.60 9.25 41.05 63.50 64.17 80.16

3.86 3.59 2.07 11.75 1.80 6.39 2.58 14.33 5.68 0.79 3.97 0.52 5.96 5.36 0.67 4.83 8.53 2.15 0.85 5.22 1.58 5.55 13.30 9.80 2.45

207.35 166.19 141.95 333.48 357.49 187.27 121.49 275.93 235.06 125.98 182.82 77.06 163.47 235.28 107.48 329.85 244.61 178.21 97.75 144.36 148.76 253.84 307.45 307.34 444.21

195.31 156.18 141.50 312.89 341.48 180.76 118.73 261.55 233.62 122.95 175.92 75.92 129.46 224.90 106.45 315.41 239.18 175.38 96.40 139.18 141.85 242.78 285.11 307.30 438.04

213.85 179.07 142.40 364.11 373.49 190.89 124.25 283.61 237.16 129.88 186.77 78.20 200.10 242.85 108.50 344.72 250.03 180.93 98.46 151.25 156.47 262.71 320.12 307.37 450.38

8.33 11.71 0.63 27.04 22.64 5.66 3.90 12.47 1.86 3.55 6.00 1.61 34.21 9.30 1.45 15.11 7.68 2.78 1.17 6.21 7.34 10.14 19.41 0.05 8.73

3 3 3

99.55 35.78 19.45

92.41 28.88 17.31

109.45 40.35 23.49

8.85 6.08 3.50

328.56 202.82 152.61

323.34 195.86 150.51

335.41 208.57 156.20

6.20 6.44 3.12

3 3

142.56 60.40

127.61 53.63

157.52 67.16

21.14 9.57

412.04 297.13

393.29 293.94

447.14 300.03

30.42 3.06

1

389.33

389.33

389.33

523.37

523.37

523.37

3 10 6

308.70 72.35 102.91

299.83 52.19 98.89

317.64 98.56 108.11

12.59 14.48 3.84

299.89 258.10 261.83

284.09 83.07 250.80

328.58 301.52 269.76

24.90 63.75 7.96

3

24.04

22.70

24.92

1.18

157.57

151.67

167.05

8.29

3

2.48

2.30

2.62

0.16

66.49

65.63

67.15

0.78

5 4 3 5 5 5 5 8

26.03 12.43 14.94 23.43 4.51 6.83 6.82 9.33

22.13 10.87 14.33 18.97 3.13 5.98 5.01 6.24

29.78 14.04 15.56 30.78 5.42 8.61 9.83 14.91

2.96 1.79 0.62 4.48 0.85 1.03 1.84 3.58

175.72 141.27 135.84 163.40 78.28 88.79 86.41 96.90

158.46 137.61 130.16 161.04 74.90 85.70 83.75 91.50

183.63 148.74 142.03 167.28 80.07 93.50 89.12 106.15

10.20 5.07 5.95 2.52 2.06 3.33 2.19 6.30

1.86 1.89 4.56

M.N. Muchlinski / Journal of Human Evolution 58 (2010) 447e473

451

Table 1 (continued ) n

Eupleridae Cryptoprocta ferox Fossa fossana Galidia elegans Felidae Felis chaus Felis concolor Felis pardalis Felis silvestris Lynx canadensis Panthera leo Panthera tigris Herpestidae Atilax paludinosus Galerella sanguinea Herpestes urva Herpestes vitticollis Ichneumia albicauda Hyaenidae Crocuta crocuta Hyaena hyaena Mephitidae Spilogale putorius Mustelidae Arctonyx collaris Conepatus rex Eira barbara Enhydra lutris Lontra canadensis Martes flavigula Melogale moschata Mustela vison Taxidea taxus Procyonidae Bassaricyon alleni Bassaricyon gabbii Bassariscus astutus Bassariscus sumichrasti Nasua nasua Potos flavus Procyon cancrivorus Procyon lotor Ursidae Ailuropoda Melanoleuca Melursus ursinus Tremarctos ornatus Ursus americanus Ursus arctos Viverridae Hemigalus derbyanus Paradoxurus hermaphroditus Chiroptera Emballonuridae Balantiopteryx plicata Cormura brevirostris Emballonura atrata Peropteryx kappleri Saccolaimus peli Saccolaimus saccolaimus Saccopteryx bilineata Taphozous nudiventris Hipposideridae Hipposideros commersoni Megadermatidae Megaderma lyra Cardioderma cor Lavia frons Molossidae Chaerephon bivittata Cynomops abrasus Eumops perotis Molossus sinaloae

IOF area

GM

Mean

Min

Max

SD

Mean

Min

Max

SD

4 3 5

16.12 7.37 3.19

13.18 6.66 2.29

20.07 8.71 3.73

3.01 1.16 0.56

93.59 64.84 52.02

91.07 63.21 49.79

96.63 67.63 54.00

2.40 2.43 1.61

5 5 5 7 7 7 6

6.98 27.57 16.72 8.33 8.97 262.50 268.00

4.52 19.98 11.67 6.82 7.31 221.69 215.40

7.92 38.41 20.58 9.24 10.56 267.27 305.51

1.64 7.23 3.38 0.99 1.24 24.04 39.35

87.34 160.91 111.32 79.00 104.16 301.53 256.45

83.33 148.48 105.54 74.76 96.15 286.02 223.96

93.70 182.44 118.67 84.01 108.54 322.29 299.12

3.93 15.71 6.19 3.76 4.69 15.59 19.78

5 5 4 3 6

10.80 2.69 5.18 6.12 5.81

8.12 2.22 4.92 4.67 4.82

12.86 3.21 5.37 7.91 6.85

1.85 0.47 0.19 1.65 0.73

78.63 47.53 72.12 74.20 73.86

74.61 43.99 70.69 71.80 68.26

83.57 49.31 73.12 78.02 77.60

4.06 2.13 1.04 3.34 3.20

5 5

19.36 22.45

16.92 19.00

23.66 28.21

2.72 3.73

200.38 186.23

186.75 170.87

216.36 192.30

10.70 8.74

5

2.69

2.16

3.15

0.39

40.10

37.71

43.26

2.09

4 5 6 4 5 5 5 8 6

233.48 4.54 11.95 42.91 41.89 9.78 25.38 8.81 28.51

198.92 3.15 9.06 29.40 31.43 7.47 23.27 5.60 24.22

274.74 5.79 14.42 51.21 50.51 11.70 26.65 11.95 34.67

31.21 1.18 2.47 9.44 6.82 1.95 1.41 2.87 4.38

118.56 60.00 89.66 112.57 87.78 65.78 59.92 48.47 102.34

112.39 46.84 83.56 104.93 85.02 60.75 56.12 44.83 101.10

124.10 66.29 95.61 118.41 92.82 70.09 63.00 53.55 105.14

5.88 7.65 5.58 6.57 2.97 4.10 2.74 4.52 1.60

6 7 7 7 17 7 8 9

5.66 6.15 8.39 7.65 10.16 10.42 26.52 11.63

4.45 5.43 6.41 6.32 6.92 9.56 21.70 9.89

6.77 6.73 11.59 9.20 18.40 11.48 30.65 15.03

1.11 0.66 2.07 1.13 3.77 0.97 4.46 2.19

64.86 63.02 61.83 65.11 92.25 70.46 105.02 85.94

64.01 62.20 57.16 52.43 80.55 68.93 100.25 82.75

65.34 63.94 67.10 73.86 103.72 73.13 115.21 89.08

0.74 0.73 3.73 8.47 7.68 1.69 6.03 2.70

2 2 3 2 5

19.62 24.20 14.41 26.99 24.34

15.93 23.37 12.84 21.85 23.28

23.30 25.02 17.12 32.13 25.96

5.21 1.17 2.36 7.27 1.17

242.49 251.70 183.91 189.16 262.01

242.15 227.09 168.28 185.91 251.03

242.82 276.30 194.98 192.40 282.59

0.47 34.80 13.92 4.59 14.08

5 5

10.28 9.31

6.29 6.72

12.56 11.18

2.41 1.91

72.59 71.52

71.16 65.41

73.73 76.47

1.16 4.20

7 5 6 8 6 7 8 5

0.41 0.38

0.23 0.20

0.58 0.67

0.18 0.17

0.81 0.38 0.22 0.68

0.72 0.25 0.10 0.54

0.89 0.51 0.31 0.84

0.09 0.09 0.08 0.11

11.12 12.62 9.85 12.91 25.16 20.44 13.20 22.52

10.86 12.07 9.47 12.80 25.01 20.12 12.54 21.85

11.30 13.06 10.21 13.06 25.32 20.64 14.06 23.17

0.20 0.43 0.37 0.14 0.22 0.21 0.55 0.61

8

2.91

2.59

3.15

0.22

26.07

25.79

26.51

0.33

8 5 7

0.59 0.56 0.74

0.39 0.33 0.41

0.74 0.67 1.07

0.13 0.14 0.25

20.73 18.79 18.47

20.09 17.68 18.24

21.30 19.51 18.77

0.45 0.77 0.27

5 4 8 8

0.96 0.93 1.35 0.46

0.85 0.86 1.07 0.28

1.16 0.98 1.65 0.63

0.13 0.06 0.23 0.14

15.66 16.96 23.17 16.65

15.39 16.80 22.74 16.38

15.92 17.13 24.28 16.88

0.21 0.14 0.64 0.21

(continued on next page)

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M.N. Muchlinski / Journal of Human Evolution 58 (2010) 447e473

Table 1 (continued ) n

IOF area Mean

Mops leucostigma Natalidae Natalus stramineus Noctilionidae Noctilio leporinus Nycteridae Nycteris thebaica Phyllostomidae Anoura geoffroyi Artibeus fraterculus Artibeus glaucus Brachyphylla cavernarum Carollia brevicauda Centurio senex Chiroderma salvini Choeronycteris mexicana Chrotopterus auritus Desmodus rotundus Glossophaga soricina Leptonycteris nivalis Macrotus waterhousii Micronycteris megalotis Mimon bennettii Monophyllus redmani Phyllostomus discolor Platalina genovensium Platyrrhinus aurarius Rhinophylla pumilio Sphaeronycteris toxophyllum Sturnira lilium Sturnira magna Tonatia saurophila Trachops cirrhosus Uroderma bilobatum Vampyressa bidens Vampyrum spectrum Pteropodidae Cynopterus horsfieldi Dobsonia minor Dobsonia moluccensis Eonycteris spelaea Epomops franqueti Harpyionycteris whiteheadi Hypsignathus monstrosus Nyctimene albiventer Paranyctimene raptor Ptenochirus jagori Pteropus conspicillatus Pteropus griseus Pteropus neohibernicus Rousettus amplexicaudatus Syconycteris australis Rhinolophidae Rhinolophus affinis Rhinolophus rufus Vespertilionidae Glauconycteris argentata Histiotus montanus Ia io Kerivoula papillosa Miniopterus schreibersii Myotis blythii Myotis nigricans Otonycteris hemprichii Scotophilus dinganii Vespadelus douglasorum Cingulata Dasypodidae Chaetophractus villosus Priodontes maximus Dasypus novemcinctus Dermoptera Cynocephalidae

Min

GM Max

SD

Max

SD

5

0.65

0.51

0.80

0.10

16.13

15.53

17.00

0.55

8

0.19

0.10

0.36

0.10

11.73

11.41

11.88

0.19

5

0.32

0.23

0.42

0.08

22.05

21.20

23.21

0.87

8

0.14

0.11

0.18

0.03

14.19

13.79

14.64

0.37

8 8 5 8 8 5 4 5 5 8 8 5 5 5 4 4 7 1 8 8 5 8 5 5 5 8 5 5

0.22 0.49 0.22 0.47 0.20 0.12 0.54 0.35 0.69 0.49 0.24 0.38 0.29 0.28 0.67 0.36 1.61 0.28 0.49 0.15 0.15 0.35 0.33 0.39 0.50 0.39 0.30 1.02

0.15 0.43 0.15 0.34 0.17 0.10 0.41 0.25 0.54 0.37 0.13 0.23 0.28 0.20 0.62 0.36 1.17 0.28 0.39 0.12 0.08 0.29 0.26 0.26 0.41 0.26 0.20 0.85

0.29 0.57 0.27 0.60 0.31 0.15 0.64 0.46 0.80 0.66 0.37 0.51 0.30 0.35 0.73 0.36 2.22 0.28 0.60 0.20 0.21 0.41 0.42 0.53 0.67 0.63 0.50 1.19

0.06 0.06 0.06 0.11 0.06 0.02 0.10 0.08 0.12 0.11 0.09 0.11 0.01 0.06 0.05

15.42 21.06 15.26 22.19 15.20 15.63 20.22 16.87 25.07 17.09 14.27 17.23 16.48 12.62 17.40 14.59 20.00 17.85 21.45 12.99 14.00 16.60 20.66 17.56 19.19 16.73 14.43 34.25

16.80 21.66 15.53 23.49 16.30 16.90 21.03 17.24 26.85 18.53 14.81 18.15 17.52 12.87 19.02 14.59 21.62 17.85 21.93 13.57 14.55 17.51 22.13 19.58 20.36 18.10 15.95 35.27

0.66 0.25 0.10 0.50 0.26 0.53 0.57 0.15 0.71 0.59 0.21 0.35 0.43 0.12 0.74

0.10 0.03 0.06 0.05 0.06 0.10 0.10 0.15 0.12 0.16

15.94 21.48 15.36 22.78 15.22 16.20 20.62 17.10 25.74 17.65 14.53 17.56 17.03 12.79 18.35 14.59 20.97 17.85 21.73 13.29 14.30 17.16 21.43 18.74 19.74 17.44 15.11 34.82

0.19 0.23 0.25 0.36 0.58 0.75 0.55 0.53 0.55 0.40

7 7 7 10 7 7 7 10 7 10 8 7 10 10 7

0.73 0.42 3.46 0.62 0.82 0.89 0.69 0.67 0.47 0.83 4.14 3.05 2.53 0.86 0.61

0.60 0.28 2.35 0.42 0.51 0.71 0.43 0.57 0.29 0.77 3.54 2.14 1.99 0.73 0.44

0.90 0.76 3.93 1.03 1.15 1.07 0.91 1.09 0.58 0.89 4.80 3.55 3.37 1.01 0.84

0.13 0.19 0.65 0.24 0.26 0.25 0.20 0.28 0.12 0.06 0.53 0.56 0.60 0.10 0.19

25.08 29.05 47.18 27.48 35.99 29.81 48.98 22.55 20.03 26.87 58.49 43.41 59.17 29.07 19.28

24.68 28.06 44.58 26.62 33.13 29.30 44.41 21.87 19.03 25.31 56.22 41.21 57.27 27.86 18.47

25.53 29.64 48.80 28.75 39.25 30.32 53.12 23.01 20.86 28.29 60.24 45.06 61.98 30.35 20.53

0.35 0.65 1.71 0.95 2.46 0.72 4.08 0.43 0.70 1.13 1.59 1.57 2.05 1.11 1.03

10 8

0.44 0.58

0.28 0.40

0.79 0.78

0.20 0.16

15.94 20.27

15.04 19.75

16.35 20.96

0.52 0.55

4 5 2 8 8 5 8 8 8 5

0.24 0.40 0.53 0.36 0.37 0.35 0.21 0.66 0.87 0.22

0.21 0.32 0.51 0.25 0.27 0.32 0.15 0.53 0.76 0.17

0.27 0.56 0.55 0.44 0.45 0.37 0.32 0.82 0.96 0.26

0.03 0.09 0.02 0.08 0.07 0.02 0.07 1.13 0.07 0.04

10.43 14.25 21.14 13.55 11.38 18.02 10.24 16.91 17.07 10.14

10.25 13.81 20.92 13.20 11.01 17.24 9.66 15.69 16.72 9.99

10.68 14.64 21.37 13.82 11.59 18.42 10.74 18.59 17.48 10.42

0.18 0.35 0.32 0.26 0.22 0.47 0.45 1.30 0.29 0.17

3 1 5

5.83 9.10 3.76

5.36 9.10 2.78

6.59 9.10 4.59

0.66

75.98 126.28 64.50

75.13 126.28 62.16

76.65 126.28 66.30

0.77

0.45

0.84

Mean

Min

0.71

1.65

M.N. Muchlinski / Journal of Human Evolution 58 (2010) 447e473

453

Table 1 (continued ) n

IOF area Mean

GM Max

SD

Cynocephalus volans Galeopterus variegatus

15 19

1.13 0.92

0.90 0.52

1.62 1.39

1.13 0.28

55.68 56.06

54.54 54.16

57.79 59.07

1.27 1.44

Erinaceomorpha Erinaceidae Atelerix algirus Atelerix frontalis Echinosorex gymnura Erinaceus europaeus Hemiechinus auritus Hylomys suillus

6 5 9 10 10 7

2.66 1.72 6.72 3.10 2.01 1.14

2.66 1.01 6.10 2.52 1.07 0.83

2.66 2.83 8.07 3.57 2.88 1.50

0.75 0.77 0.42 0.82 0.24

41.55 38.28 59.29 41.27 35.65 24.46

41.55 37.05 56.35 38.91 32.06 21.99

41.55 39.69 63.97 44.94 38.54 27.31

1.11 2.68 2.51 3.26 2.24

4 5

3.04 4.89

2.76 3.51

3.65 5.80

0.42 0.84

61.40 69.57

56.47 66.12

65.14 71.53

3.61 2.23

7 2 1 1 8 8

2.92 2.32 2.31 1.63 2.36 6.33

2.46 2.07 2.31 1.63 1.88 6.33

3.96 2.56 2.31 1.63 2.92 6.33

0.60 0.35

54.62 37.09 60.01 42.37 46.04 54.56

51.26 35.42 60.01 42.37 44.88 52.90

56.44 38.77 60.01 42.37 46.88 56.31

1.98 2.37

0.90 1.30

8

1.98

1.32

2.68

0.63

28.82

27.73

29.64

0.87

2

396.86

355.72

438.00

58.18

450.48

419.52

481.43

43.77

3 3

175.60 105.69

162.56 100.63

182.32 114.47

20.31 7.64

305.54 249.66

303.35 239.47

306.77 260.15

1.91 10.34

5

0.72

0.42

0.93

0.26

50.28

48.48

54.20

2.29

5

0.65

0.38

0.81

0.17

33.73

31.94

35.54

1.36

5

3.21

2.23

4.50

0.89

86.12

79.98

97.83

7.83

6

5.14

3.98

6.44

1.02

148.82

143.02

156.31

6.82

5 5 7 4 5 5 4

1.27 1.18 1.26 2.09 1.42 1.81 1.55

0.87 1.03 0.87 1.45 0.91 1.15 1.32

1.43 1.30 1.53 2.30 1.98 2.38 2.03

0.23 0.10 0.30 0.43 0.41 0.57 0.33

49.46 48.85 48.27 50.25 49.26 49.22 49.86

48.15 47.35 46.61 49.83 47.51 47.71 49.40

50.81 49.67 51.11 50.75 50.73 50.64 50.41

1.10 1.01 2.11 0.38 1.44 1.23 0.52

6 8 6 9 7 6 10 15

2.53 1.84 2.63 2.23 2.03 2.43 1.93 2.34

2.09 1.43 1.79 1.40 1.45 2.28 1.23 1.09

3.90 2.19 3.18 3.13 2.71 2.68 2.59 4.34

0.77 0.32 0.74 0.62 0.60 0.16 0.50 1.12

90.36 88.76 91.76 96.02 87.87 88.55 72.97 83.98

83.50 83.46 83.68 86.31 83.99 84.68 27.48 79.51

103.21 96.71 97.37 105.77 90.84 95.30 88.19 89.16

7.62 6.14 7.17 9.04 2.73 4.13 25.54 3.29

9 8 6 15 15 10 7 7 8 2 8

0.62 0.82 0.61 0.51 0.47 3.12 2.88 2.65 1.07 0.96 0.53

0.56 0.67 0.45 0.35 0.34 2.59 1.89 2.53 0.53 0.95 0.35

0.67 0.92 0.95 0.66 0.74 3.10 3.76 2.79 1.40 0.97 0.71

0.04 0.10 0.20 0.10 0.12 0.50 0.81 0.12 0.35 0.01 0.14

42.03 37.10 38.08 34.71 27.29 77.99 79.79 79.46 44.51 40.94 37.95

40.56 35.92 37.12 30.03 22.77 75.62 74.31 72.86 44.30 40.18 35.50

42.99 37.94 39.56 36.60 28.67 81.43 82.47 85.37 44.76 41.70 39.16

0.91 0.79 1.04 2.01 1.69 2.25 3.76 6.28 0.23 1.07 1.56

Hyracoidea Procaviidae Heterohyrax brucei Procavia capensis Lagamorpha Leporidae Oryctolagus cuniculus Poelagus marjorita Pronolagus randensis Romerolagus diazi Sylvilagus audubonii Lepus americanus Ochotonidae Ochotona princeps Perissodactyla Rhinocerotidae Rhinoceros unicornis Tapiridae Tapirus indicus Tapirus terrestris Pilosa Bradypodidae Bradypus variegatus Cyclopedidae Cyclopes didactylus Megalonychidae Choloepus didactylus Myrmecophagidae Myrmecophaga tridactyla Primates Aotidae Aotus azarai Aotus infulatus Aotus lemurinus Aotus nancymaae Aotus nigriceps Aotus trivirgatus Aotus vociferans Atelidae Alouatta belzebul Alouatta caraya Alouatta palliata Alouatta seniculus Ateles belzebuth Ateles fusciceps Ateles geoffroyi Lagothrix lagotricha Cebidae Callimico goeldii Callithrix argentata Callithrix humeralifer Callithrix jacchus Callithrix pygmaea Cebus albifrons Cebus apella Cebus capucinus Leontopithecus rosalia Saguinus bicolor Saguinus fuscicollis

Min

Max

SD

0.37

Mean

Min

(continued on next page)

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M.N. Muchlinski / Journal of Human Evolution 58 (2010) 447e473

Table 1 (continued ) n

IOF area Mean

Saguinus geoffroyi Saguinus imperator Saguinus inustus Saguinus midas Saguinus mystax Saguinus oedipus Saimiri boliviensis Saimiri oerstedii Saimiri sciureus Cercopithecidae Cercocebus albigena Cercocebus ascanius Cercopithecus diana Cercopithecus erythrotis Cercopithecus mitis Cercopithecus nictitans Cercopithecus talapoin Chlorocebus aethiops Colobus badius Colobus guereza Colobus rufomitratus Colobus satanas Erythrocebus patas Macaca assamensis Macaca fascicularis Macaca mulatta Macaca nemestrina Nasalis larvatus Papio anubis Papio hamadryas Presbytis entellus Pygathrix nemaeus Rhinopithecus roxellana Theropithecus gelada Trachypithecus obscurus Cheirogaleidae Cheirogaleus major Cheirogaleus medius Microcebus murinus Mirza coquereli Phaner furcifer Daubentoniidae Daubentonia madagascariensis Galagidae Galago alleni Galago demidoff Galago moholi Galago senegalensis Otolemur crassicaudatus Otolemur garnettii Euoticus elegantulus Galago matschiei Hominidae Gorilla beringei Gorilla gorilla Homo sapiens Pan paniscus Pan troglodytes Pongo pygmaeus Hylobatidae Hylobates agilis Hylobates lar Hylobates muelleri Nomascus concolor Indriidae Avahi laniger Indri indri Propithecus diadema Propithecus verreauxi Lemuridae Eulemur coronatus Eulemur fulvus Eulemur macaco Eulemur mongoz

Min

GM Max

SD

Max

SD

8 8 7 9 7 3 5 4 13

1.32 1.03 0.94 0.85 0.77

0.80 0.85 0.68 0.76 0.61

1.60 1.12 1.33 0.92 1.02

0.29 0.10 0.22 0.08 0.18

43.46 41.48 41.73 40.16 43.04

42.37 40.33 39.96 39.35 42.50

44.24 42.81 42.94 41.10 43.63

0.95 0.89 1.03 0.83 0.52

1.22 1.33 0.66

0.96 1.17 0.50

1.50 1.46 0.89

0.24 0.15 0.15

48.08 46.83 49.54

44.87 44.65 44.52

51.30 47.77 53.55

2.34 1.46 3.54

6 10 3 1 10 6 4 8 7 4 5 1 11 5 8 10 7 16 7 8 6 8 5 8 7

1.37 1.14 3.76 2.54 1.65 2.59 1.26 2.52 1.83 1.81 3.04 2.43 2.76 3.82 3.38 1.61 4.51 3.12 7.55 3.31 4.81 1.66 4.37 7.24 2.15

1.09 0.82 3.71 2.54 1.04 2.36 0.84 1.67 1.43 0.90 2.81 2.43 1.22 2.50 2.37 1.14 2.61 2.12 6.10 2.38 3.75 1.23 3.59 6.36 1.74

1.99 1.55 3.81 2.54 2.09 2.76 1.75 3.36 2.58 2.71 3.59 2.43 3.94 4.87 5.36 2.09 6.11 4.28 10.11 3.71 6.43 2.32 5.82 8.37 2.39

0.36 0.31 0.07

89.07 78.38 79.08 82.22 91.55 92.81 58.83 77.68 96.02 96.31 86.70 94.83 98.16 103.07 88.47 87.51 107.42 102.51 149.53 134.01 109.65 92.38 100.87 135.83 82.88

93.64 72.00 74.35 82.22 86.75 90.47 55.15 67.64 83.73 88.78 80.89 94.83 86.40 93.70 82.45 83.31 96.06 88.80 129.13 106.95 96.06 86.91 95.01 126.14 80.51

102.99 83.27 83.82 82.22 96.40 94.14 61.80 90.26 103.57 103.83 95.83 94.83 112.02 113.59 96.04 92.71 117.82 113.20 162.31 150.56 117.77 99.37 106.72 146.53 85.91

3.78 4.42 6.69

6 6 13 3 4

1.49 1.01 0.57 1.15 1.15

1.27 0.95 0.39 1.15 0.82

1.71 1.12 0.78 1.15 1.37

0.31 0.08 0.14 0.29

45.18 35.48 25.60 43.97 39.40

44.93 34.38 24.91 43.97 36.92

45.43 36.06 26.21 43.97 41.88

3.51

5

2.58

1.99

2.94

0.43

71.29

67.64

75.72

3.80

1 15 5 15 15 7 4 1

0.44 0.33 0.53 0.35 1.56 1.28 0.65 0.31

0.44 0.20 0.32 0.24 0.74 0.92 0.54 0.31

0.44 0.42 0.79 0.51 2.35 1.91 0.70 0.31

0.06 0.19 0.08 0.50 0.44 0.07

43.33 28.42 32.47 32.96 56.55 55.88 39.93 35.51

43.33 26.49 29.92 27.57 36.88 52.62 38.20 35.51

43.33 30.85 34.28 37.18 64.26 57.34 40.94 35.51

1.34 1.84 3.12 7.96 2.19 1.51

3 15 4 1 20 13

10.31 9.64 7.81 5.75 8.26 11.64

7.81 4.51 5.50 5.75 4.16 7.35

13.05 14.25 9.47 5.75 13.32 14.51

1.91 2.89

219.56 214.28 156.74 144.81 157.69 172.03

197.30 210.78 153.56 144.81 143.19 152.82

233.04 220.60 161.56 144.81 171.15 199.11

4 21 7 7

2.84 4.82 3.93 2.56

2.84 3.20 2.05 1.79

2.84 8.40 5.09 3.92

1.41 1.39 0.97

82.43 85.98 83.47 83.94

82.43 80.68 79.66 82.68

82.43 91.48 86.01 84.90

3.03 2.93 1.09

8 7 6 12

0.54 1.06 1.00 1.83

0.27 0.78 0.70 0.79

0.96 1.43 1.55 2.77

0.24 0.31 0.39 0.70

44.34 80.03 74.00 66.19

43.33 79.03 70.84 63.46

46.06 81.27 76.16 69.19

1.02 0.94 2.40 1.81

7 13 17 7

1.62 1.68 2.27 1.17

1.12 0.44 1.01 1.12

1.94 2.34 3.15 1.21

0.33 0.65 0.70 0.06

61.68 66.58 68.56 60.20

59.04 63.51 62.47 58.58

64.26 70.35 71.83 61.82

2.61 2.23 3.56 2.29

0.39 0.18 0.37 0.68 0.44 1.28 0.42 1.00 0.98 1.18 0.36 1.67 0.74 1.61 0.63 1.00 0.47 0.86 0.82 0.30

2.63 2.90 1.93

Mean

Min

4.61 1.54 2.76 9.03 8.72 10.64 5.99 9.21 8.36 6.62 3.71 10.14 9.17 15.98 23.62 8.28 5.78 8.27 9.59 2.32 0.35 0.95 0.49

19.42 5.48 4.24 8.42 18.41

M.N. Muchlinski / Journal of Human Evolution 58 (2010) 447e473

455

Table 1 (continued ) n

IOF area Mean

Eulemur rubriventer Hapalemur griseus Lemur catta Varecia variegata Lepilemuridae Lepilemur mustelinus Lorisidae Arctocebus calabarensis Loris tardigradus Nycticebus coucang Nycticebus pygmaeus Perodicticus potto Pitheciidae Cacajao calvus Cacajao melanocephalus Callicebus brunneus Callicebus cupreus Callicebus moloch Chiropotes albinasus Chiropotes satanas Pithecia aequatorialis Pithecia monachus Tarsiidae Tarsius bancanus Tarsius syrichta Tarsius tarsier Rodentia Anomaluridae Anomalurus beecrofti Anomalurus derbianus Aplodontiidae Aplodontia rufa Castoridae Castor canadensis Castor fiber Caviidae Cavia tschudii Chinchillidae Lagidium viscacia Cricetidae Abrothrix longipilis Cricetulus migratorius Lemmus sibiricus Microtus arvalis Myodes gapperi Neotoma fuscipes Ondatra zibethicus Phyllotis xanthopygus Holochilus sciureus Microtus subterraneus Ctenodactylidae Massoutiera mzabi Pectinator spekei Ctenomyidae Ctenomys magellanicus Dasyproctidae Myoprocta acouchy Dipodidae Allactaga sibirica Allactaga bullata Jaculus jaculus Zapus hudsonius Erethizontidae Coendou rothschildi Geomyidae Cratogeomys gymnurus Geomys pinetis Thomomys bottae Gliridae Glis glis Muscardinus avellanarius Heteromyidae

Min

GM Max

SD

Mean

Min

Max

SD

9 9 12 15

1.54 0.83 1.32 1.96

0.92 0.61 0.49 0.91

2.14 1.03 2.16 3.56

0.56 0.13 0.48 0.76

67.21 51.90 64.06 78.61

65.45 50.22 61.07 74.18

71.09 53.88 67.27 81.56

2.30 1.35 1.96 2.24

8

0.52

0.46

0.58

0.04

42.10

40.21

46.84

2.45

3 15 14 5 13

0.73 0.36 1.16 0.94 1.39

0.73 0.20 0.83 0.66 0.95

0.73 0.50 1.65 1.13 1.90

0.09 0.33 0.20 0.36

40.81 38.65 49.90 43.01 54.59

40.81 29.78 45.97 42.45 51.24

40.81 41.65 56.64 43.75 57.82

3.76 4.11 0.59 1.80

8 6 4 5 8 3 6 4 12

3.19 3.00 1.66 1.28 1.19 1.64 2.59 2.06 1.39

2.98 2.78 1.37 1.05 0.91 1.60 1.97 1.45 1.21

3.38 3.32 2.07 1.66 1.52 1.71 3.33 2.68 1.60

0.18 0.28 0.31 0.23 0.25 0.06 0.60 0.64 0.18

79.93 76.79 51.28 50.11 50.14 69.19 71.89 67.56 67.06

76.25 75.36 50.30 47.11 48.61 67.00 70.09 63.64 63.45

83.75 78.42 52.51 52.01 52.96 72.92 73.45 70.52 70.36

3.26 1.54 0.99 1.99 1.66 3.25 1.60 2.94 2.01

5 8 9

0.41 0.34 0.39

0.31 0.26 0.31

0.50 0.41 0.55

0.13 0.06 0.10

36.61 34.72 29.96

36.52 33.00 28.69

36.70 35.58 30.90

0.13 1.02 0.93

2 3

24.13 22.43

20.39 18.50

27.86 25.49

5.28 3.58

46.10 48.87

44.32 45.79

47.87 51.95

2.51 4.36

7

10.66

7.12

14.56

2.80

61.17

55.61

66.91

5.04

16 1

10.64 14.49

6.02 14.49

18.43 14.49

3.99

111.88 114.91

101.76 114.91

126.00 114.91

8.12

5

163.12

154.49

181.31

10.49

40.68

39.63

42.18

0.99

5

209.55

168.99

245.00

27.55

59.70

57.25

62.58

2.09

5 3 5 5 5 5 5 5 5 5

3.51 3.86 5.43 5.29 3.37 1.93 3.54 11.26 21.89 5.45

2.47 3.08 3.92 4.76 2.41 1.47 2.22 9.82 18.78 4.55

4.86 5.41 6.50 6.09 4.67 2.18 5.20 13.88 25.41 6.21

1.00 1.34 1.05 0.54 0.82 0.28 1.26 1.89 2.97 0.67

22.35 20.18 26.79 26.08 20.00 16.91 16.95 34.75 49.59 21.98

21.70 19.25 23.66 24.81 19.08 16.56 16.48 34.08 47.96 21.29

23.40 21.88 28.75 27.41 20.73 17.55 17.58 36.12 50.47 22.53

0.70 1.48 1.95 1.17 0.61 0.42 0.44 0.87 0.96 0.54

3 2

21.89 26.32

19.86 25.42

24.61 27.22

2.45 1.27

36.14 35.24

33.74 34.66

38.67 35.82

2.46 0.82

5

35.02

27.21

41.13

5.22

38.85

34.49

42.72

3.67

5

130.37

118.52

144.84

12.97

57.72

55.39

58.61

1.32

8 5 9 3

0.84 0.73 1.00 5.55

0.72 0.59 0.79 5.06

1.07 0.88 1.34 5.89

0.14 0.13 0.24 0.43

28.93 28.27 26.58 15.50

28.26 27.10 26.16 15.03

29.23 29.30 27.01 15.98

0.41 0.94 0.35 0.48

5

86.29

78.29

88.84

4.51

58.16

54.52

61.40

3.25

7 7 7

2.33 1.68 1.25

1.66 0.74 1.02

3.29 2.01 1.35

0.71 0.54 0.14

52.44 37.45 32.31

47.40 34.05 29.01

57.23 41.21 36.29

4.27 3.37 2.74

6 4

2.40 1.94

1.44 1.78

3.23 2.10

0.79 0.23

27.28 17.31

26.88 16.93

27.75 17.68

0.44 0.54

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Table 1 (continued ) n

IOF area Mean

Dipodomys merriami Dipodomys ordii Heteromys desmarestianus Perognathus fasciatus Muridae Aethomys kaiseri Calomys sorellus Carpomys phaeurus Chrotomys whiteheadi Crateromys schadenbergi Cricetomys emini Dipodillus campestris Hydromys chrysogaster Leopoldamys sabanus Meriones crassus Otomys irroratus Phloeomys pallidus Rattus rattus Reithrodontomys megalotis Rhombomys opimus Sundamys infraluteus Nesomyidae Cricetomys emini Eliurus grandidieri Nesomys rufus Petromyscus collinus Petromyscus shortridgei Sciuridae Callosciurus caniceps Callosciurus erythraeus Callosciurus finlaysoni Callosciurus flavimanus Callosciurus notatus Callosciurus prevostii Callosciurus pygerythrus Cynomys ludovicianus Dremomys pernyi Dremomys rufigenis Funisciurus lemniscatus Glaucomys sabrinus Glaucomys volans Hylopetes alboniger Hylopetes phayrei Marmota flaviventris Marmota monax Menetes berdmorei Microsciurus flaviventer Paraxerus ochraceus Paraxerus palliatus Petaurista petaurista Petinomys maerens Protoxerus stangeri Ratufa affinis Ratufa bicolor Sciurotamias davidianus Sciurus aberti Sciurus apache Sciurus carolinensis Sciurus colliaei Sciurus niger Spermophilus leptodactylus Spermophilus beecheyi Spermophilus columbianus Spermophilus richardsonii Spermophilus spilosoma Spermophilus tridecemlineatus Sundasciurus hippurus Tamias amoenus Tamias bulleri Tamias minimus Tamiasciurus hudsonicus Tamiops macclellandi Xerus erythropus Xerus rutilus

Min

GM Max

SD

Mean

Min

Max

SD

6 7 7 7

5.29 5.32 3.18 1.44

4.19 3.22 1.75 0.59

7.00 6.52 4.54 2.83

1.36 1.82 1.47 0.91

27.45 29.98 23.10 16.26

25.75 29.57 20.96 14.65

28.66 30.43 24.93 17.25

0.99 0.33 1.90 1.00

8 5 1 5 6 4 8 4 8 9 8 3 8 5 5 4

7.17 2.96 5.03 4.35 20.63 23.45 2.98 10.67 14.10 4.64 8.46 17.02 4.76 2.12 7.78 14.22

4.79 1.17 5.03 2.35 15.78 17.48 2.57 8.83 8.48 4.19 6.18 13.30 4.13 1.70 6.16 11.57

8.72 3.63 5.03 6.07 27.68 26.44 3.36 12.47 17.84 4.88 11.42 21.55 5.86 2.38 9.11 16.36

1.70 1.04

25.57 17.47 28.76 24.28 50.22 41.03 21.24 33.91 34.87 28.34 26.74 59.35 25.12 13.98 29.76 42.98

27.50 18.96 28.76 30.51 52.23 51.20 22.76 37.57 39.74 30.20 30.73 63.29 27.95 14.92 33.07 44.52

0.82 0.68

1.35 6.25 4.04 0.35 1.82 3.60 0.26 1.94 4.18 0.66 0.28 1.22 2.16

26.60 18.23 28.76 27.42 51.22 47.51 21.90 35.74 36.71 29.60 29.36 61.35 25.87 14.58 31.35 43.62

2.55 1.43 4.52 0.64 2.59 1.81 0.78 1.55 1.97 1.39 0.39 1.50 0.75

1 5 5 3 3

13.14 3.57 10.79 2.24 3.26

13.14 3.14 9.08 1.84 2.57

13.14 3.86 11.67 2.49 3.70

0.27 1.00 0.35 0.60

48.85 24.97 31.66 18.06 17.95

48.85 24.56 30.49 17.92 17.53

48.85 25.21 32.42 18.16 18.32

0.27 0.87 0.12 0.40

10 10 10 7 5 7 7 10 9 10 4 10 10 5 7 7 10 7 12 10 10 7 5 10 10 9 10 9 7 10 7 10 9 10 10 8 10 10 7 6 7 7 10 10 10 7

1.72 2.04 1.78 2.23 1.37 2.55 1.56 3.51 1.49 2.02 1.08 0.80 0.65 1.76 1.36 3.81 3.45 1.69 1.42 1.14 1.19 2.25 1.18 9.02 2.17 2.56 1.55 2.53 2.12 2.06 2.24 3.02 2.15 3.04 2.14 1.57 1.51 2.12 2.22 1.87 1.64 1.38 1.62 0.53 2.12 2.26

1.34 1.71 1.24 1.58 1.15 2.10 1.19 2.75 0.84 1.58 1.02 0.65 0.51 1.00 0.92 2.46 2.91 1.12 1.07 0.78 0.90 1.68 1.03 6.06 1.62 2.10 1.26 2.09 1.79 1.49 1.94 2.10 1.85 2.75 1.50 1.07 1.20 1.61 1.83 1.34 1.22 1.13 1.46 0.32 1.78 2.12

1.98 2.46 2.02 2.71 1.56 3.15 1.90 4.70 2.12 2.30 1.14 1.00 0.77 2.51 1.68 6.16 3.91 2.34 1.98 1.73 1.41 2.76 1.30 11.19 3.17 3.15 1.73 2.78 2.36 2.36 2.53 3.71 2.52 3.45 2.79 1.95 1.70 2.67 2.67 2.44 1.91 1.56 1.73 0.67 2.41 2.39

0.26 0.29 0.32 0.48 0.18 0.40 0.31 0.84 0.46 0.29 0.08 0.13 0.10 1.07 0.27 1.49 0.44 0.54 0.35 0.38 0.24 0.39 0.14 2.12 0.61 0.43 0.23 0.28 0.25 0.35 0.22 0.67 0.28 0.30 0.47 0.36 0.21 0.48 0.32 0.51 0.29 0.16 0.10 0.15 0.24 0.12

36.82 41.23 41.38 43.44 36.60 43.05 34.96 50.71 38.05 40.70 33.69 28.93 25.11 41.61 30.22 62.95 66.02 36.32 28.92 29.74 38.35 57.74 36.66 51.84 52.26 54.89 41.27 45.49 48.11 45.72 45.01 50.99 43.02 45.40 40.70 37.17 31.91 33.70 42.38 25.00 27.66 22.95 36.63 24.68 45.84 40.03

14.45 40.46 39.39 42.34 35.40 42.03 34.03 48.24 36.90 39.28 31.12 28.59 24.59 41.48 29.26 53.51 62.56 35.81 28.14 28.95 36.11 53.16 35.71 51.19 51.34 52.52 39.96 43.50 44.11 44.56 44.21 47.10 42.50 41.18 38.47 35.01 30.91 32.52 40.90 24.69 25.78 22.26 35.64 24.49 45.16 35.92

44.55 41.56 42.39 44.02 37.68 44.08 35.81 52.60 39.75 42.56 36.27 29.31 26.29 41.74 30.95 73.44 69.70 36.86 29.86 30.36 39.65 59.62 37.61 52.71 53.59 56.94 42.12 47.18 49.82 46.53 45.99 54.26 43.54 47.59 43.30 39.11 32.95 34.42 44.12 25.30 28.50 23.81 37.82 25.07 46.55 42.10

12.66 0.46 1.19 0.64 0.94 0.73 0.82 2.21 1.55 1.25 3.64 0.28 0.69 0.18 0.67 9.20 2.97 0.44 0.62 0.51 1.56 2.68 1.34 0.59 0.83 2.22 0.82 1.53 2.38 0.82 0.74 3.30 0.59 2.63 1.87 1.69 0.94 0.71 1.59 0.26 1.10 0.56 0.83 0.23 0.62 2.40

M.N. Muchlinski / Journal of Human Evolution 58 (2010) 447e473

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Table 1 (continued ) n

Spalacidae Rhizomys pruinosus Scandentia Ptilocercidae Ptilocercus lowii Tupaiidae Anathana ellioti Dendrogale melanura Tupaia dorsalis Tupaia glis Tupaia gracilis Tupaia javanica Tupaia minor Tupaia montana Tupaia palawanensis Tupaia tana Soricomorpha Solenodontidae Solenodon paradoxus Soricidae Anourosorex squamipes Blarina brevicauda Blarinella quadraticauda Chimarrogale himalayica Nectogale elegans Neomys fodiens Scutisorex somereni Sorex araneus Sorex cinereus Suncus megalura Suncus murinus Crocidura flavescens Crocidura hildegardeae Crocidura russula Cryptotis goodwini Talpidae Condylura cristata Desmana moschata Scalopus aquaticus Scaptonyx fusicaudus Talpa europaea Metatherian Dasyuromorphia Dasyuridae Dasyuroides byrnei Dasyurus hallucatus Dasyurus maculatus Dasyurus viverrinus Antechinus flavipes Antechinus swainsonii Phascogale calura Planigale maculata Sarcophilus laniarius Sminthopsis butleri Sminthopsis crassicaudata Didelphidae Caluromys derbianus Caluromys lanatus Caluromys philander Chironectes minimus Didelphis albiventris Didelphis marsupialis Glironia venusta Marmosa murina Marmosa rubra Metachirus nudicaudatus Monodelphis domestica Philander andersoni Philander opossum Thylamys elegans Lutreolina crassicaudata

IOF area

GM

Mean

Min

Max

SD

Mean

Min

Max

SD

5

21.28

16.44

22.99

2.85

57.27

52.80

61.46

3.38

2

0.98

0.97

0.98

0.01

27.63

27.63

27.63

6 11 10 15 7 8 15 8 15 12

0.44 0.45 0.56 0.75 1.01 0.69 0.68 0.82 0.79 0.64

0.39 0.00 0.45 0.38 0.42 0.54 0.48 0.56 0.51 0.40

0.47 0.83 0.80 1.08 1.30 0.89 0.94 1.28 1.14 0.89

0.03 0.35 0.11 0.28 0.41 0.17 0.12 0.28 0.24 0.16

30.49 24.32 32.38 33.77 28.54 29.51 26.45 35.27 33.98 38.01

29.85 23.19 30.69 32.32 27.91 28.05 25.52 33.99 32.66 35.95

30.92 25.28 33.52 34.58 29.83 30.09 27.66 36.01 35.82 40.82

0.56 0.77 1.31 0.64 0.87 0.84 0.81 0.80 1.00 1.44

8

7.22

2.67

5.17

1.38

51.87

48.20

54.02

2.21

5 10 5 3 6 11 7 10 7 10 10 7 8 10 4

2.94 0.77 1.79 3.72 5.86 0.99 1.20 0.31 0.41 0.68 1.32 0.86 1.40 0.51 2.34

2.48 0.52 1.31 3.54 5.38 0.73 0.90 0.27 0.35 0.57 1.06 0.80 1.01 0.34 2.01

3.56 0.99 2.14 3.99 6.46 1.39 1.37 0.39 0.48 0.92 1.56 0.91 2.01 0.72 2.81

0.48 0.17 0.31 0.24 0.42 0.29 0.18 0.05 0.05 0.14 0.20 0.05 0.42 0.14 0.42

17.89 16.65 13.72 19.09 19.20 15.29 20.21 14.20 11.98 12.05 20.16 17.90 12.97 13.25 15.72

17.46 16.29 13.43 18.27 18.71 15.02 19.50 13.75 11.27 11.69 19.73 16.25 12.61 12.82 15.51

18.25 17.02 13.89 19.65 19.64 15.51 20.80 14.35 12.58 12.40 20.79 18.86 13.49 13.90 15.94

0.30 0.30 0.17 0.72 0.40 0.20 0.60 0.26 0.54 0.31 0.49 1.44 0.33 0.43 0.22

8 3 13 5 17

1.06 3.11 0.99 0.47 1.13

1.02 3.01 0.64 0.40 0.71

1.14 3.20 1.54 0.50 1.34

0.05 0.13 0.31 0.05 0.26

21.13 40.39 24.56 16.16 23.52

20.47 40.39 21.31 16.00 22.31

21.36 40.39 27.08 16.25 25.27

0.37

8 9 9 3 4 10 1 1 5 3 7

1.92 2.77 6.08 2.51 0.75 1.41 0.76 0.34 15.41 0.67 0.51

1.67 2.39 5.47 2.48 0.66 1.26 0.76 0.34 14.11 0.60 0.35

2.36 2.96 6.42 2.54 0.81 1.58 0.76 0.34 16.84 0.81 0.69

0.27 0.26 0.42 0.04 0.06 0.12

33.39 48.86 79.57 51.50 22.61 22.05 25.19 13.93 98.51 16.89 17.85

31.56 47.41 78.52 50.05 22.45 20.85 25.19 13.93 96.89 16.31 17.03

35.54 50.66 80.63 52.96 22.80 22.57 25.19 13.93 98.92 17.38 18.70

15 12 13 12 13 10 1 15 5 15 8 5 10 8 8

2.02 1.92 1.57 3.95 3.72 3.59 1.18 0.67 0.78 1.61 1.14 2.45 2.71 0.78 3.28

1.40 1.45 1.27 2.54 2.78 2.89 1.18 0.56 0.59 1.18 0.87 2.08 2.30 0.65 2.18

2.75 2.49 1.82 4.89 4.69 4.10 1.18 0.91 0.98 1.87 1.42 3.01 3.20 0.98 4.19

43.70 44.13 39.11 54.40 62.85 72.39 26.17 26.45 26.96 36.13 31.18 47.99 47.36 22.40 47.40

39.89 41.03 36.20 50.40 53.98 68.43 26.17 24.20 24.23 33.20 27.57 46.21 46.06 21.05 40.38

47.25 46.35 42.60 58.76 70.74 81.36 26.17 29.14 29.30 40.55 33.89 48.72 49.09 23.06 54.02

1.17 0.12 0.12 0.44 0.32 0.19 0.79 0.73 0.46 0.12 0.15 0.21 0.22 0.37 0.39 0.14 0.79

2.37 0.12 0.83

1.46 1.34 1.50 2.06 0.17 0.72

1.09 0.54 0.67 2.29 1.76 2.45 3.00 6.28 4.32 1.28 1.87 2.06 2.66 1.19 1.30 0.91 5.56

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Table 1 (continued ) n

IOF area Mean

Myrmecobiidae Myrmecobius fasciatus Thylacinidae Thylacinus cynocephalus

Min

GM Max

SD

Min

Max

SD

41.60

40.32

42.89

1.08

10

1.43

1.12

1.90

1

43.25

43.25

43.25

139.87

139.87

139.87

1 1

0.61 0.32

0.61 0.32

0.61 0.32

20.75 16.07

20.75 16.07

20.75 16.07

4 7 5 2 2 5 4 2 10 13

3.12 3.77 3.39 3.80 0.70 10.32 3.60 3.20 3.65 3.33

2.84 3.33 2.73 3.08 0.70 9.02 3.18 2.85 2.29 2.27

3.40 4.53 3.86 4.51 0.70 11.81 4.02 3.54 5.42 5.17

1.15 0.59 0.49 1.20 1.25

84.63 87.86 82.45 85.95 56.27 123.27 74.65 71.22 64.56 75.17

82.82 83.32 80.98 82.79 56.27 119.83 71.57 68.38 59.90 71.54

86.43 91.37 85.18 89.10 56.27 125.16 77.74 74.06 68.17 78.06

2.36 4.36 4.02 2.98 2.68

1 2 7 15

1.75 1.52 3.45 2.56

1.75 1.52 2.87 1.23

1.75 1.52 3.89 3.86

0.39 0.96

48.06 48.85 42.62 30.80

48.06 48.85 41.44 27.32

48.06 48.85 44.02 34.69

1.03 2.25

3 1 1 10 5 8 17

2.59 2.42 3.03 2.23 4.79 2.87 2.40

2.22 2.42 3.03 1.65 4.00 2.28 1.79

3.25 2.42 3.03 3.01 4.89 3.28 3.10

0.57 0.08 0.44 0.48

77.47 56.77 76.47 64.80 79.52 67.34 60.71

73.97 56.77 76.47 60.15 72.42 66.21 56.97

80.18 56.77 76.47 75.03 87.71 70.12 64.20

4.61 7.34 1.87 2.36

5

3.66

2.59

4.95

0.98

106.99

102.78

112.71

4.98

8 7 12

3.05 2.29 1.97

2.42 2.11 1.49

3.57 2.46 2.58

0.44 0.15 0.46

64.60 56.74 62.32

61.95 55.93 55.30

68.06 57.54 68.33

2.20 0.61 4.77

7 9 8

1.43 1.21 1.92

1.32 0.93 1.80

1.60 1.42 2.03

0.12 0.20 0.10

45.47 42.19 53.35

44.65 41.11 51.95

46.30 44.11 55.28

0.63 1.24 1.49

2

3.06

1.77

4.34

1.82

15.31

15.01

15.61

0.42

2 9

20.52 11.50

18.05 9.78

22.98 12.90

3.49 1.14

134.89 140.53

132.12 136.16

137.66 144.22

3.92 3.69

2

5.59

4.60

6.57

1.39

91.42

90.47

92.37

1.34

5 5 5

1.69 1.02 4.20

1.28 0.87 3.49

2.30 1.32 4.66

0.40 0.18 0.49

25.38 26.67 47.13

24.10 25.88 45.36

26.24 27.19 48.04

0.86 0.48 1.08

Microbiotheria Microbiotheriidae Dromiciops gliroides

5

0.34

0.28

0.43

0.06

20.80

19.54

22.31

1.23

Notoryctemorphia Notoryctidae Notoryctes typhlops

4

1.30

0.69

1.90

0.86

20.88

20.82

20.93

0.08

Paucituberculata Caenolestidae Caenolestes fuliginosus Lestoros inca Rhyncholestes raphanurus

5 5 3

0.59 1.22 0.91

0.39 0.94 0.67

0.72 1.44 1.13

0.14 0.20 0.23

21.49 20.90 20.91

20.68 20.33 20.32

22.25 21.51 21.39

0.68 0.56 0.54

5 14 8 8

2.78 1.73 2.87 2.75

2.10 1.16 2.59 2.34

3.19 2.04 3.26 3.56

0.42 0.35 0.28 0.49

44.64 46.98 53.11 49.29

38.08 44.32 50.39 48.14

53.58 51.24 54.76 50.70

6.44 2.71 1.89 1.05

Diprotodontia Burramyidae Cercartetus caudatus Cercartetus nanus Macropodidae Dendrolagus bennettianus Dendrolagus inustus Dendrolagus lumholtzi Dorcopsis hageni Lagorchestes hirsutus Macropus robustus Petrogale lateralis Petrogale penicillata Setonix brachyurus Thylogale billardierii Petauridae Dactylopsila palpator Dactylopsila trivirgata Petaurus australis Petaurus breviceps Phalangeridae Ailurops ursinus Phalanger carmelitae Phalanger gymnotis Phalanger orientalis Spilocuscus maculatus Trichosurus caninus Trichosurus vulpecula Phascolarctidae Phascolarctos cinereus Potoroidae Aepyprymnus rufescens Bettongia penicillata Potorous tridactylus Pseudocheiridae Hemibelideus lemuroides Petauroides volans Pseudochirops cupreus Tarsipedidae Tarsipes rostratus Vombatidae Lasiorhinus latifrons Vombatus ursinus Macropodidae Diprotodontia Wallabia bicolor Macroscelididae Elephantulus rufescens Macroscelides proboscideus Rhynchocyon cirnei

Peramelemorphia Peramelidae Echymipera kalubu Isoodon obesulus Perameles gunnii Perameles nasuta

0.30

Mean

0.40 0.46 0.59 1.01

0.57

2.55 4.07 2.37 4.46

3.18

M.N. Muchlinski / Journal of Human Evolution 58 (2010) 447e473

459

Table 1 (continued ) n

IOF area Mean

Thylacomyidae Macrotis lagotis

1

3.82

Min 3.82

GM Max 3.82

SD

Mean

Min

Max

60.63

60.63

60.63

SD

Infraorbital foramen area (IOF) and geometric mean (GM) of cranial length and width for 527 mammal species. Number of specimens (n), area averages (averages, in mm2); minimum area (min); maximum area (max); and standard deviation (SD) values are indicated.

primates. All orders had adequate power (>0.80) and could therefore be compared with primates. Mystacial vibrissa count comparisons: Vibrissa count comparisons were conducted two ways. The first comparison investigated how macro, micro, and total vibrissa counts differ between primates and non-primate mammals, while the second comparison examined differences in these counts between strepsirrhines and haplorhines. To test for differences in relative macro, micro, and total vibrissa counts between (1) non-primate mammals and primates, and (2) haplorhines and strepsirrhines, the natural log of each vibrissa count variable was regressed against ln GM, and an ANCOVA (significance set at p < 0.05) was used to test for differences in vibrissa counts (with GM as covariate). Mystacial vibrissae and infraorbital foramen area correlation: A Spearman’s rank correlation was used to test the relationship between ln macro-vibrissae, ln micro-vibrissae, ln total vibrissae, and ln IOF area among (1) all mammals, and (2) primates. The hystricomorphous and myomorphous rodents were excluded from this analysis. A Mahalanobis distance plot was used to identify outliers. Mahalanobis distances metrically addresses the question of whether or not a particular data point, or species in this case, would be considered an outlier relative to a particular set of group data (Zar, 1999). Any species in this sample that has a greater Mahalanobis distance from the rest of the sample population is considered to have higher leverage, and thus a greater influence, on the correlation coefficient (Zar, 1999). Independent contrasts: Because closely related species are more likely to share anatomical similarities than distantly related species, phylogeny must be considered. Phylogenetically independent contrasts (PICs) were calculated using the PDAP:PDTREE module (Midford et al., 2008) of Mesquite version 1.07 (Maddison and Maddison, 2007). Contrast data were calculated using a tree with equal branch lengths, a method that was shown to be robust by Martins and Garland (1991). The mammalian phylogenetic supertree was constructed from a number of published sources: mammalian supraordinal and ordinal relationships (Springer et al., 2004; Nishihara et al., 2006); Chiroptera (Simmons and Geisler, 1998; Giannini and Simmons, 2003; Teeling et al., 2005; Dumont, 2007); Xenarthra and Hyracoidea (Delsuc et al., 2002); Artiodactyla and Persidactyla (Matthee and Robinson, 1999; Agnarsson and May-Collado, 2008); Erinaceomorpha, Afrosoricida, and Soricomorpha (Grenyer and Purvis, 2003; Ohdachi et al., 2006; Gilbert, 2008); Carnivora (BinindaEmonds et al., 1999); Rodentia and Lagomorpha (Steppan et al., 2004, 2005; Horner et al., 2007); Scandentia (Olson et al., 2005; Kriegs et al., 2007); Dermoptera (Jane cka et al., 2007; Kriegs et al., 2007); Primates (Primates overall: Purvis, 1995; Strepsirrhini: Roos et al., 2004; Platrrhini: Opazo et al., 2006; and Catarrhini: Xing et al., 2005; Steiper and Young, 2006); and Metatheria (Cardillo et al., 2004). The first set of analyses used the PICs to compare differences between clades. Specifically, I tested for differences between the

calculated contrasts for relative IOF area and vibrissa count (macro, micro, and total) of (1) Primates and all other mammals, (2) Primatomorpha and all other mammals, (3) Euarchonta and all other mammals, and (4) the primate suborders. To control for the effects of body mass, independent contrasts of the dependent variables (IOF area, and macro, micro, and total vibrissae counts) were regressed on positivized contrasts in GM, using a least squares regression forced through the origin (see Garland et al., 1999). The residual values from these analyses represent sizeadjusted contrasts. To test the hypothesis that a particular clade is grade shifted from its sister group, a t-test was used to determine whether particular outliers (e.g., Euarchonta vs. all other mammals node) fall more than two standard deviations from the regression line. The second group of analyses explored the proposed relationship between macro-vibrissa, micro-vibrissa, and total vibrissa count and IOF area. A Pearson product-moment correlation was used to test the relationships between contrast IOF area and each of contrast macro, micro, and total vibrissa count. Results Infraorbital foramen area variation among mammals Observed differences between primates and non-primate mammals (excluding hystricomorphous and myomorphous rodents) were statistically significant when considered in an ANCOVA (p < 0.001, F ¼ 218.72, r2 ¼ 0.78; Fig. 2A). The IOFs of primates are approximately 37% smaller than those of most nonprimate mammals, based on the reported differences in y-intercept. This finding did not change when the data were analyzed using independent contrasts (t ¼ 1.95; p ¼ 0.05, Fig. 2B). Primates have relatively smaller IOFs than all non-primate eutherians (ANCOVA: p < 0.001; F ¼ 224.41; r2 ¼ 0.80) and metatherians as a group (ANCOVA: p < 0.001; F ¼ 157; r2 ¼ 0.79). Convex polygons fit around the relative IOF area values for primates and all other mammalian orders show there is very little overlap between these primates and most other mammals (Fig. 3). Although the majority of non-primate mammalian orders do cluster around one another, several orders deviate notably from the mammalian cluster (Fig. 3). These outliers are the two rodent suborders (Hystricomorpha and Myomorpha), the two orders that belong to the supraorder Xenarthra (Cingulata and Pilosa), Scandentia, and Dermoptera (Fig. 3). Euarchontans (ANCOVA: p < 0.001; F ¼ 247.40; r2 ¼ 0.79), but not Euarchontoglires, have significantly smaller relative IOFs than most other mammals. These findings did change when the data were analyzed using independent contrasts. Contrast data indicate that Primatomorpha (t ¼ 2.2; p ¼ 0.03), but not Euarchontans (t ¼ 1.56; p ¼ 0.12), were significantly different from other mammals (Fig. 2A). When relative IOF area values for all primates were compared to each mammalian order separately, results of a Wilcoxon Rank Sum test indicate that primates did not significantly differ from four eutherian and three metatherian orders (Table 3).

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M.N. Muchlinski / Journal of Human Evolution 58 (2010) 447e473

Table 2 Macro- and micro-vibrissa counts for 238 mammal species. n

Macro-vibrissae Mean

Min

Max

Micro-vibrissae SD

Mean

Min

Max

SD

16 16 12 12 21 15

20 21 15 19 21 20

2.31 2.52 1.53 3.79 2.65

Afrosoricida Tenrecidae Echinops telfairi Geogale aurita Hemicentetes semispinosus Microgale talazaci Potamogale velox Tenrec ecaudatus

3 3 3 3 1 3

21 26 15 38 64 19

19 23 13 36 64 16

21 29 16 40 64 19

1.73

16 18 14 18 21 16

Artiodactyla Suidae Sus barbatus

2

13.5

12

15

2.12

51.5

51

52

0.71

3

24

19

27

4.04

18

16

22

3.06

2 2 2 3 1

25 25 22 31 27

22 25 21 28 27

27 25 22 36 27

3.54 0.00 0.71 4.04

27 27 20 12 49

27 25 16 10 49

27 30 24 12 49

0.00 3.33 5.66 1.15

2 3 1

10 27 15

10 26 15

10 30 15

0.00 2.08

40 37 34

40 37 34

41 41 34

0.71 2.30

3 1 2

24 24 27

23 24 26

24 24 28

0.58

50 17 22

49 17 22

52 17 23

1.53

1

e

e

e

27

27

27

Carnivora Canidae Vulpes vulpes Felidae Felis concolor Felis silvestris Lynx canadensis Panthera leo Panthera tigris Mustelidae Eira barbara Mustela vison Taxidea taxus Procyonidae Nasua nasua Procyon cancrivorus Procyon lotor Ursidae Ursus arctos Chiroptera Emballonuridae Balantiopteryx plicata Emballonura atrata Peropteryx kappleri Saccolaimus peli Saccopteryx bilineata Hipposideridae Hipposideros commersoni Megadermatidae Megaderma lyra Molossidae Eumops perotis Molossus sinaloae Natalidae Natalus stramineus Nycteridae Nycteris thebaica Phyllostomidae Anoura geoffroyi Artibeus fraterculus Brachyphylla cavernarum Carollia brevicauda Desmodus rotundus Glossophaga soricina Monophyllus redmani Phyllostomus discolor Platyrrhinus aurarius Rhinophylla pumilio Sturnira lilium Uroderma bilobatum Pteropodidae Eonycteris spelaea Harpyionycteris whiteheadi Nyctimene albiventer Ptenochirus jagori Pteropus conspicillatus Pteropus neohibernicus Rousettus amplexicaudatus Rhinolophidae Rhinolophus affinis

1.15 3.00 1.53 2.00

1.41 e

0.71

3 3 3 3 3

4 3 5 5 3

3 2 4 3 3

4 3 5 5 3

0.58 0.58 0.58 1.15 0.00

4 4 3 4 4

3 2 3 4 4

4 4 5 4 5

0.58 1.15 1.15 0.00 0.58

3

7

6

10

2.08

9

6

11

2.52

3

7

3

9

3.06

12

10

12

1.15

3 3

5 2

4 2

6 3

1.00 0.58

5 3

3 0

6 3

1.53 1.73

3

4

3

4

0.58

3

3

4

0.58

3

3

2

3

0.58

10

8

12

2.00

3 3 3 3 3 3 3 3 3 3 3 3

7 10 9 8 6 7 8 8 10 5 8 7

7 9 7 6 5 7 8 6 7 5 7 7

8 11 9 9 7 7 9 10 11 5 8 9

0.58 1.00 1.15 1.53 1.00 0.00 0.58 2.00 2.08 0.00 0.58 1.15

11 9 10 10 8 8 9 11 10 9 7 6

10 8 9 8 7 7 8 3 10 7 5 5

12 11 12 11 8 8 12 12 11 9 8 6

1.00 1.53 1.53 1.53 0.58 0.58 2.08 4.93 0.58 1.15 1.53 0.58

3 3 3 3 1 3 3

13 11 13 12 21 5 9

12 11 13 12 21 5 9

14 12 16 12 21 8 9

1.00 0.58 1.73 0.00

7 11 7 9 20 5 11

12 13 10 11 20 7 14

2.52 1.00 1.53 1.00

1.73 0.00

9 12 8 10 20 5 12

3

6

6

6

0.00

8

7

9

1.00

1.15 1.52

M.N. Muchlinski / Journal of Human Evolution 58 (2010) 447e473

461

Table 2 (continued ) n

Macro-vibrissae Mean

Max

SD

5

5

5

0.00

10

8

10

1.15

3 3 3 3 3

4 5 6 7 5

3 4 6 6 4

4 6 6 8 5

0.58 1.00 0.00 1.00 0.58

3 3 8 4 4

3 3 7 4 3

3 4 9 6 5

0.00 0.58 1.00 0.57 1.00

Cingulata Dasypodidae Dasypus novemcinctus

2

7

7

8

0.71

14

11

18

4.95

Dermoptera Cynocephalus volan Galeopterus variegates

4 5

20 18

16 16

23 21

2.94 1.87

17 10

5 8

25 19

8.41 4.87

Erinaceomorpha Erinaceidae Atelerix algirus Erinaceus europaeus Hemiechinus auritus

2 3 3

13 15 14

13 14 14

14 15 15

0.71 0.58 0.58

27 20 22

23 20 19

32 22 22

6.36 1.56 1.73

2 3 3

16 29 29

16 25 27

17 31 31

0.71 3.06 2.00

12 17

9 12

16 19

3.51 3.61

3

21

20

27

3.79

15

14

22

4.36

3 3 3

22 23 25

20 20 17

23 24 35

1.53 2.08 9.02

20 17 19

20 16 17

23 24 24

1.73 4.36 3.61

1 3 3 2 2 1 3 3

18 17 29 14 29 30 19 33

18 16 23 14 26 30 12 11

18 19 29 15 32 30 26 34

37 27 18 23 24 25 31 31

37 26 15 22 24 25 22 8

37 31 24 24 24 25 34 31

2 3 1 3 3 3 3 3 3 3 3 3 2 3 3 6

16 15 17 11 11 26 17 8 15 13 13 12 17 14 11 46

13 14 17 9 10 25 17 3 15 12 11 10 15 9 10 40

19 20 17 13 13 32 24 15 19 14 15 14 20 19 13 54

10 12 13 17 10 35 32 30 10 17 9 10 21 8 18 23

9 12 13 12 7 34 19 29 7 8 9 10 19 6 18 22

11 15 13 25 10 37 26 30 11 17 14 10 23 10 19 34

5 1 3 1 1 3 2 3 3 3 3 3 3

40 33 31 31 33 29 31 30 42 35 46 28 33

37 33 29 31 33 26 30 30 40 35 38 20 33

43 33 36 31 33 34 32 32 65 39 46 32 40

32 40 36 33

32 40 35 33

32 40 40 33

39 23 52 36 52 43 42 31

34 20 48 30 52 42 32 28

54 25 56 41 55 45 46 32

Lagamorpha Leporidae Oryctolagus cuniculus Sylvilagus audubonii Lepus americanus Ochotonidae Ochotona princeps Primates Aotidae Aotus lemurinus Aotus nigriceps Aotus trivirgatus Atelidae Alouatta belzebul Alouatta caraya Alouatta palliata Alouatta seniculus Ateles belzebuth Ateles fusciceps Ateles geoffroyi Lagothrix lagotricha Cebidae Callimico goeldii Callithrix argentata Callithrix humeralifer Callithrix jacchus Callithrix pygmaea Cebus albifrons Cebus apella Cebus capucinus Leontopithecus rosalia Saguinus fuscicollis Saguinus geoffroyi Saguinus imperator Saguinus midas Saguinus mystax Saguinus oedipus Saimiri sciureus Cercopithecidae Cercocebus ascanius Cercopithecus diana Cercopithecus mitis Cercopithecus nictitans Cercopithecus talapoin Chlorocebus aethiops Colobus guereza Erythrocebus patas Macaca assamensis Macaca fascicularis Macaca mulatta Macaca nemestrina Nasalis larvatus

Max

Micro-vibrissae

3

Rhinolophus rufus Vespertilionidae Kerivoula papillosa Miniopterus schreibersii Myotis nigricans Otonycteris hemprichii Scotophilus dinganii

Min

SD

1.53 3.78 0.71 4.24 7.00 13.00 4.24 3.21 2.00 1.53 2.00 4.04 6.03 2.31 1.00 2.00 2.00 3.54 5.00 1.53 4.80 4.23 3.61

4.04 1.41 1.15 13.89 2.31 4.61 6.11 4.04

Mean

Min

2.64 4.58 1.41 0.00 6.24 13.28 1.41 1.73 6.56 1.73 1.53 1.53 0.58 2.08 5.20 2.89 0.00 2.83 2.00 0.58 4.62

2.65

10.41 3.54 4.00 5.51 3.62 2.12 7.21 2.08

(continued on next page)

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M.N. Muchlinski / Journal of Human Evolution 58 (2010) 447e473

Table 2 (continued ) n

Papio hamadryas Presbytis entellus Pygathrix nemaeus Theropithecus gelada Trachypithecus obscurus Cheirogaleidae Cheirogaleus major Microcebus murinus Galagidae Galago demidoff Galago moholi Galago senegalensis Otolemur crassicaudatus Otolemur garnettii Hominidae Gorilla gorilla Pan troglodytes Pongo pygmaeus Hylobatidae Hylobates agilis Hylobates lar Hylobates muelleri Nomascus concolor Lemuridae Eulemur fulvus Eulemur macaco Eulemur mongoz Eulemur rubriventer Lemur catta Varecia variegata Lorisidae Arctocebus calabarensis Loris tardigradus Nycticebus coucang Perodicticus potto Pitheciidae Cacajao calvus Cacajao melanocephalus Callicebus cupreus Callicebus moloch Chiropotes satanas Pithecia aequatorialis Pithecia monachus Tarsiidae Tarsius bancanus Tarsius syrichta Tarsius tarsier Rodentia Castoridae Castor canadensis Dipodidae Jaculus jaculus Muridae Aethomys kaiseri Crateromys schadenbergi Dipodillus campestris Hydromys chrysogaster Leopoldamys sabanus Meriones crassus Otomys irroratus Rattus rattus Sciuridae Callosciurus caniceps Callosciurus erythraeus Callosciurus finlaysoni Cynomys ludovicianus Dremomys pernyi Dremomys rufigenis Glaucomys sabrinus Glaucomys volans Hylopetes alboniger Marmota monax Microsciurus flaviventer

Macro-vibrissae Mean

Min

Max

3 1 3 3 3

59 41 52 53 28

58 41 52 45 28

61 41 62 57 32

2 3

19 21

17 19

3 3 3 3 3

11 16 19 22 22

2 5 2

Micro-vibrissae SD

Mean

Min

Max

SD

53 33 36 50 33

62 33 45 60 39

2.83

5.77 6.11 2.31

57 33 39 58 33

4.58 5.29 3.46

22 22

3.54 1.53

6 12

5 9

7 12

1.41 1.73

10 15 19 10 22

11 18 24 26 25

0.58 1.53 2.89 8.33 1.73

12 9 11 10 12

10 7 10 10 10

13 13 14 15 12

1.53 3.06 2.08 2.89 1.15

0 0 0

0 0 0

0 0 0

0.00 0.00 0.00

12 22 59

10 17 54

15 23 64

3.54 2.51 7.07

3 3 2 2

39 27 30 25

34 21 30 23

40 34 30 27

3.21 6.51 0.00 2.85

29 34 33 27

25 28 31 27

31 34 35 35

3.06 3.46 2.83 5.68

1 5 3 2 2 3

36 40 34 28 29 37

36 31 24 25 28 33

36 44 45 31 31 43

6.12 10.50 4.24 2.12 5.03

14 14 14 12 9.5 12

14 11 13 10 9 11

14 17 16 15 10 16

2.77 1.53 3.54 0.71 2.65

2 3 3 2

7 12 25 24

7 10 23 22

7 15 29 27

0.00 2.52 3.06 3.54

7 5 15 13

6 5 15 11

8 6 20 15

1.41 0.58 2.89 2.83

3 3 3 1 2 3 2

25 19 22 19 19 16 9

23 18 21 19 18 11 8

27 21 24 19 20 17 11

2.00 1.53 1.53

26 30 22 26 24 28 27

25 29 21 26 16 23 25

26 32 24 26 33 28 30

0.58 1.53 1.53

3 3 1

12 15 17

11 15 17

12 19 17

0.58 2.31

14 11 15

12 11 15

16 12 15

2.00 0.58

4

21

19

23

1.62

26

24

26

1.15

3

59

54

65

5.51

53

53

54

4.93

3 3 3 1 3 3 3 3

32 37 45 55 41 43 52 39

27 34 38 55 40 34 50 35

35 38 46 55 45 44 53 40

4.04 2.06 4.36

34 35 27 12 37 21 26 30

34 30 26 12 33 20 23 27

38 37 30 12 40 25 27 33

2.31 3.61 2.08

3 3 3 3 2 3 3 3 1 3 5

27 23 23 27 21 21 25 25 20 23 24

27 23 22 23 20 19 23 23 20 23 20

30 25 23 27 23 21 25 25 20 23 24

1.73 1.15 0.58 2.31 2.12 1.15 1.15 1.15

23 26 18 26 26 16 16 12 24 35 20

23 23 18 25 25 14 14 9 24 31 18

29 26 25 27 27 16 17 15 24 40 23

3.46 1.73 4.04 1.00 1.41 1.15 1.53 3.00

1.73

1.41 3.21 2.12

2.65 5.51 1.53 2.65

0.00 1.79

12.02 2.89 3.54

3.51 2.65 2.08 3.00

6.36 1.95

M.N. Muchlinski / Journal of Human Evolution 58 (2010) 447e473

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Table 2 (continued ) n

Paraxerus ochraceus Paraxerus palliatus Protoxerus stangeri Ratufa affinis Ratufa bicolor Sciurotamias davidianus Sciurus aberti Sciurus carolinensis Sciurus niger Spermophilus leptodactylus Spermophilus beecheyi Spermophilus columbianus Spermophilus richardsonii Spermophilus spilosoma Spermophilus tridecemlineatus Tamiasciurus hudsonicus Tamiops macclellandi Xerus erythropus Tupaiidae Dendrogale melanura Tupaia glis Tupaia javanica Tupaia minor Tupaia montana Tupaia palawanensis Solenodontidae Solenodon paradoxus Soricidae Blarina brevicauda Neomys fodiens Sorex araneus Suncus megalura Suncus murinus Crocidura hildegardeae Crocidura russula Talpidae Condylura cristata Scalopus aquaticus Scaptonyx fusicaudus Talpa europaea Metatherian Dasyuromorphia Dasypodidae Dasyuroides byrnei Dasyurus hallucatus Dasyurus maculatus Dasyurus viverrinus Antechinus swainsonii Didelphidae Caluromys derbianus Caluromys lanatus Caluromys philander Didelphis albiventris Didelphis marsupialis Marmosa murina Metachirus nudicaudatus Monodelphis domestica Philander opossum Thylamys elegans Lutreolina crassicaudata Myrmecobiidae Myrmecobius fasciatus Macropodidae Thylogale billardierii Petauridae Dactylopsila trivirgata Petaurus breviceps Phalangeridae Phalanger orientalis Trichosurus caninus Trichosurus vulpecula Phascolarctidae

Macro-vibrissae Mean

Min

Max

3 3 3 3 2 3 2 3 3 3 3 3 1 3 3 3 3 3

22 21 21 21 23 27 22 21 20 23 25 19 16 17 17 25 21 13

21 21 19 20 22 26 22 21 19 20 23 16 16 16 16 21 20 13

22 22 21 25 25 28 23 22 20 23 27 20 16 17 18 26 23 14

2 3 1 3 3 3

15 11 15 14 14 22

14 11 15 13 13 19

17 15 15 14 15 24

1

42

42

42

3 4 3 3 3 1 3

38 57 57 53 43 76 38

36 52 56 53 42 76 36

45 60 58 56 44 76 40

3 3 1 3

15 8 19 16

12 6 19 16

17 9 19 20

1 5 3 1 3

39 30 33 26 28

39 30 24 26 25

39 38 34 26 35

3 2 1 3 3 3 3 3 3 3 1

34 26 25 22 26 23 25 25 25 23 23

32 24 25 20 19 21 25 23 24 22 23

34 28 25 23 28 24 29 26 25 23 23

1

8

8

8

3

26

25

26

1 3

15 19

15 18

3 2 5

20 35 37

19 32 32

Micro-vibrissae SD

Mean

Min

Max

SD

21 22 26 24 45 27 24 25 20 20 29 16 20 17 15 18 13 18

19 10 24 23 44 22 22 22 20 19 28 15 20 16 14 18 11 18

22 27 28 26 46 28 26 28 23 22 32 18 20 17 16 19 15 18

1.53 8.74 2.83 1.53 1.41 3.21 2.83 3.00 1.73 1.53 2.08 1.53

29 6 12 8 18 12

28 5 12 6 10 10

30 10 12 8 18 15

56

56

56

19 35 16 20 16 28 17

16 30 13 19 16 28 15

20 35 17 23 16 28 20

24 37 36 34

21 36 36 32

25 38 36 38

22 23 27 21 19

22 22 26 21 16

22 29 29 21 25

15 14 16 19 22 16 17 17 15 16 17

10 14 16 19 20 15 12 15 13 13 17

15 14 16 20 26 19 20 17 15 17 17

8

8

8

0.58

29

26

30

2.08

15 19

0.58

17 14

17 13

17 17

2.08

22 39 37

1.53 4.95 2.89

20 35 29

20 35 29

24 35 49

2.31 0.00 5.48

0.58 0.58 1.15 2.65 2.12 1.00 0.71 0.58 0.58 1.73 2.00 2.08 0.58 1.00 2.65 1.53 0.58 2.12 2.31 0.58 1.00 2.52

4.73 3.30 1.00 1.73 1.00 2.00 2.52 1.53 2.31

3.49 5.51 5.13 1.15 2.83 1.53 4.73 1.53 2.31 1.53 0.58 0.58

0.58 1.00 0.58 2.00 0.00 1.41 2.65 1.15 4.62 2.52

2.08 2.50 2.08 2.08 0.00 2.52 2.08 1.41 3.06

2.92 1.52 4.58 2.89 0.00 0.58 3.06 2.08 4.04 1.15 1.15 2.08

(continued on next page)

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Table 2 (continued ) n

Phascolarctos cinereus Potoroidae Aepyprymnus rufescens Bettongia penicillata Potorous tridactylus Pseudocheiridae Hemibelideus lemuroides Petauroides volans Pseudochirops cupreus Vombatidae Vombatus ursinus Peramelidae Isoodon obesulus Perameles gunnii Perameles nasuta

Macro-vibrissae

Micro-vibrissae

Mean

Min

Max

1

29

29

29

3 2 2

25 28 23

25 26 23

33 30 23

2 4 3

24 32 39

24 31 37

4

58

3 3 1

e 15 17

SD

Mean

Min

Max

10

10

10

SD

4.62 2.83 0.00

15 19 17

11 18 16

15 20 19

2.31 1.41 2.12

25 37 42

0.71 2.83 2.52

16 22 22

14 17 21

18 24 30

2.83 3.10 4.93

52

60

3.56

50

48

53

9.39

e 13 17

e 18 17

e 2.52

11 10 9

7 9 9

14 14 9

2.88 2.65

Macro- and micro-vibrissa counts for 238 mammal species. Data include number of specimens (n), mean, minimum count (min), maximum count (max), and standard deviation (SD). Vibrissa count values are from one half of the face. A value of zero (0) indicates no vibrissae were present, and a dash (e) indicates that no data could be collected for that specimen.

Cingulata, Dermoptera, Microbiotheria, Pilosa, Proboscidea, Macropodidae, and Notoryctemorphia did not differ from primates (Table 3). It is noteworthy that, although scandentians did overlap with the primate distribution (Fig. 3), they have significantly larger IOFs than primates (Z ¼ 3.02, p ¼ 0.0025). However, like primates, scandentians have relatively smaller IOFs than most non-primate mammals (Table 3). In essence, the IOFs of scandentians are intermediate in size between most non-primate mammals and primates. When all non-primate mammals were removed from the sample, there was nearly complete overlap in the relative IOF area values for strepsirrhines and haplorhines (Fig. 4A). When a least squares regression was fit to all strepsirrhines and haplorhines, there were no significant differences in slope and y-intercept (p ¼ 0.08; F ¼ 3.52; r2 ¼ 0.83) between the two suborders (Fig. 4A). This finding did not change when independent contrast data were considered (t ¼ 0.22; p ¼ 0.82; Fig. 4B). Mystacial vibrissa count comparisons An ANCOVA indicated that primates do not significantly differ from non-primate mammals in relative macro (p ¼ 0.48; F ¼ 0.50; r2 ¼ 0.50), micro (p ¼ 0.09; F ¼ 2.9; r2 ¼ 0.34), and total (p ¼ 0.08; F ¼ 3.10; r2 ¼ 0.57) vibrissa counts (Fig. 5A). Independent contrast analysis found that primates, as a group, do not significantly differ from most other mammals in macro, micro, or total vibrissa count (macro-vibrissae: t ¼ 0.72; p ¼ 0.47; micro-vibrissae: t ¼ 1.01, p ¼ 0.32; total vibrissa count: t ¼ 0.77; p ¼ 0.44). When vibrissa counts were compared between haplorhines and strepsirrhines, an ANCOVA showed no significant differences in macro (p ¼ 0.09; F ¼ 3.02; r2 ¼ 0.44) or total (p ¼ 0.26; F ¼ 1.30; r2 ¼ 0.67) vibrissa counts (Fig. 5B). The LS regression slopes for micro-vibrissa counts for haplorhines and strepsirrhines were statistically different (p < 0.0001; F ¼ 39.18; r2 ¼ 0.63). Therefore, the micro-vibrissa count LS regression line for haplorhines could not be compared to the LS regression line for strepsirrhines because the micro-vibrissa count did not meet ANCOVA assumptions. However, based on the bivariate plot of ln micro-vibrissae and ln GM, strepsirrhines as a group appear to have relatively fewer micro-vibrissae than haplorhines (Fig. 6). However, when the PIC data were considered, no differences were found in macro, micro, or total vibrissa count (macrovibrissae: t ¼ 0.87, p ¼ 0.47; micro-vibrissae: t ¼ 1.81, p ¼ 0.24; total vibrissa count: t ¼ 0.79; p ¼ 0.43).

Mystacial vibrissae and infraorbital foramen area correlation All but two species sampled possessed mystacial vibrissae. Homo sapiens and Myrmecophaga tridactyla (the giant anteater) had no macro- or micro-vibrissae, and were therefore excluded from all analyses (Table 2). The non-human hominids sampled (Gorilla gorilla, Pan troglodytes, and Pongo pygmaeus) all have microvibrissae, but lack macro-vibrissae (Table 1). Therefore, they were not included in the analysis comparing macro-vibrissa counts to IOF area. However, they were included in the analysis comparing total vibrissa counts to IOF area. When all mammals were included in the correlation analysis, the ln macro, ln micro, and ln total vibrissa counts were significantly and positively correlated with ln IOF area (macro-vibrissae: r ¼ 0.40; p < 0.001; micro-vibrissae: r ¼ 0.57; p < 0.001; total vibrissa count: r ¼ 0.54; p < 0.001) (total vibrissae: Fig. 7A). A PIC analysis yielded similar results (macro-vibrissae: r ¼ 0.24; p < 0.001; micro-vibrissae: r ¼ 0.30; p < 0.001; total vibrissa count: r ¼ 0.30; p < 0.001). This correlation was strongest between ln IOF and ln micro-vibrissa count, and weakest between ln IOF area and ln macro-vibrissa count. Total vibrissa count explains 28% (ln total vibrissa count ¼ 3.46 þ 0.27 ln IOF area, r2 ¼ 0.28) of the variation in IOF area, while macro-vibrissa count explains 20% (ln macro-vibrissa ¼ 2.80 þ 0.26 ln IOF, r2 ¼ 0.20) and micro-vibrissa count explains 30% (ln micro-vibrissa ¼ 2.68 þ 0.30 ln IOF, r2 ¼ 0.30) of the variation in IOF area. Beyond humans and the giant anteater, there were a few other notable outliers identified by the Mahalanobis distance plot for macro, micro, and total vibrissa counts, including the Hildegarde’s shrew (Crocidura hildegardeae), the common Eurasian shrew (Sorex araneus), the crab eating raccoon (Procyon cancrivorus), and the American badger (Taxidea taxus); the majority of these outliers are chiropterans (Fig. 7A). For the correlation of micro-vibrissa count and IOF area, the long-tailed mole (Scaptonyx fusicaudus), the American badger (T. taxus), and the crab eating raccoon (P. cancrivorus) all fell outside the Mahalanobis density ellipse. In the correlation comparing total vibrissa count to IOF area, the common Eurasian shrew (S. araneus), the Hildegarde’s shrew (C. hildegardeae), the American badger (T. taxus), the crab eating raccoon (P. cancrivorus), the striped civet (Fossa fossana), the Chinese ferret badger (Melogale moschata), and the lowland gorilla (G. gorilla) were identified as outliers (Fig. 7A). When all non-primate mammals were removed from the sample a significant correlation was observed between each vibrissa count variable and ln IOF area, (macro-vibrissae: r ¼ 0.57;

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Fig. 2. (A) A scatter plot illustrating the relationship among all mammals (metatherian mammals ; eutherian mammals ; primates: strepsirrhines B, and primates: haplorhines C) in ln infraorbital foramen area and ln GM (cranial length and width). Each symbol represents a species mean. A least squares (solid lines) and reduced major axis (dashed line) regression is fit to all primates and to all non-primate mammals. Hystricomorpha and Myomorpha were excluded from the regression analysis, but the xenarthrans were included because they do not have any anatomical peculiarities that would preclude them from being compared to other mammals. (B) A scatter plot illustrating the relationship among all mammals in contrast infraorbital foramen area and contrast GM (cranial length and width). The primate and Primatomorpha nodes are significantly different from the other mammalian nodes.

p < 0.001; micro-vibrissae: r ¼ 0.66; p < 0.001; total vibrissa count: r ¼ 0.58; p < 0.001) (Total vibrissae: Fig. 7B). The correlation coefficients were slightly higher for these correlations than those including all mammals. When phylogeny was considered, contrast macro, micro, and total vibrissa count each correlate significantly with contrast IOF area (macro-vibrissae: r ¼ 0.18; p ¼ 0.05; micro-vibrissae: r ¼ 0.41; p < 0.001; total vibrissa count: r ¼ 0.24; p < 0.001). For primates, macro-vibrissa counts explain approximately 21% of the variation in IOF area (ln macrovibrissae ¼ 3.00 þ 0.36 ln IOF area, r2 ¼ 0.21), while the number of micro-vibrissae accounts for approximately 21% (ln microvibrissae ¼ 2.80 þ 0.44 ln IOF area, r2 ¼ 0.40), and total vibrissa number accounts for approximately 22% (ln total vibrissa

count ¼ 3.63 þ 0.28 ln IOF area, r2 ¼ 0.22) of the variation in IOF area. The correlation for primates found that the only outliers for macro-vibrissa count were the South American squirrel monkey (Saimiri sciureus), the Calabar angwantibo (Arctocebus calabarensis), and the white-headed capuchin (Cebus capucinus). For the microvibrissa count and IOF area correlation, the greater dwarf lemur (Cheirogaleus major), the common chimpanzee (P. troglodytes), and the lowland gorilla (G. gorilla) were outliers (Fig. 7B). Outliers identified in the correlation between total vibrissa count and IOF area were the great apes, the orangutan (P. pygmaeus), the common chimpanzee (P. troglodytes), and the lowland gorilla (G. gorilla) (Fig. 7B).

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Fig. 3. Convex polygons drawn around species means values of ln infraorbital foramen area and ln GM (cranial length and width). The large rodent polygon includes the two rodent suborder outliers, Hystricomorpha and Myomorpha. The majority of rodents cluster with all non-primate mammals in the black polygon. Xenarthrans are the located in the convex polygon below primate distribution.

Discussion Infraorbital foramen variation among mammals The relative size of the IOF varies significantly across mammalian orders, but most species within an order share a similar distribution and cluster together. The convex polygons that were fit around the distributions of each taxonomic order overlapped significantly, but a grade shift in relative IOF area between most non-primate mammals and primates was documented. The data indicate that primates have a 37% reduction in IOF area compared to most other mammals. Kay and Cartmill (1977) and Martin (1999) both found a similar reduction in IOF area for primates. Kay and Cartmill (1977) also documented that metatherians have relatively larger IOFs than primates, but relatively smaller IOFs than the non-primate eutherians in their sample. A few metatherian orders in the present study did not differ from primates in relative IOF area. These orders are the Macropodids (kangaroos and wallabies), Notoryctemorphia (the marsupial mole, one of two species within this order was sampled), and Dromiciops gliroides, which is the only species in the order Microbiotheria. Although no significant differences in relative IOF area were detected between three metatherian orders and Primates, the remaining five metatherian orders sampled (Dasyuromorphia, Didelphimorphia, Diprotodontia, Paucituberculata, and Peramelemorphia) did differ significantly from Primates by having relatively larger IOFs. Despite differences in sample size between this study and Kay and Cartmill’s (1977) analysis of a much smaller sample, both studies reveal similar grade shifts between the sampled metatherians and primates. Beyond the metatherian orders mentioned above, there are a few eutherian orders that did not differ significantly from primates in relative IOF area. These groups include the sloths, anteaters, and armadillos (superorder: Xenarthra; orders: Pilosa and Cingulata), flying lemurs (Dermoptera), and elephants (Proboscidea). Of these taxa, the xenarthrans are the only group that appears to have smaller foramina than primates, but this observed trend is not statistically significant. In addition to these mammalian orders, Scandentia also shows a reduction in IOF area. Scandentians have significantly larger IOFs than primates, but they have smaller IOFs than most other mammals (based on nonPIC data). Scandentians and primates significantly differ from all of the same mammalian orders. The majority of the sampled scandentian species fell at the upper limits of the primate

distribution and below the non-primate mammal cluster in the plot showing the distribution of relative IOF area (Figs. 2A and 3). These findings are intriguing because scandentians, along with dermopterans, are the closest living relatives of primates. Together these three orders comprise the superorder Euarchonta (Kriegs et al., 2007). Based on a PIC analysis, euarchontans do not have relatively smaller IOF areas than most other non-euarchontan mammals, but primates and dermopterans as a group (Primatomoprha) did differ from most other mammals. The raw data show that there seems to be a general trend towards IOF reduction among euarchontans, and that IOF area may be an informative feature in limited phylogenetic analyses of extinct euarchontans. Currently, the exact phylogenetic affiliation of these three orders is unresolved, but three possible hypotheses have Table 3 Results of a Wilcoxon Rank Sums analysis comparing relative infraorbital foramen area of primates and scandentians across orders. Primates

Afrosoricida Artiodactyla Carnivora Chiroptera Cingulata Erinaceomorpha Dermoptera Hyracoidea Lagamorpha Macroscelidea Microbiotheria Perissodactyla Pilosa Primata Proboscidea Rodentia Scandentia Soricomorpha Dasyuromorphia Didelphimorphia Diprotodontia Macropodidae Notoryctemorphia Paucituberculata Peramelemorphia

Scandentia

Significance

Z-score

Significance

Z-score

<0.0001 <0.0001 <0.0001 <0.0001 0.33 <0.0001 0.27 0.016 <0.0001 0.02 0.46 0.003 0.86

5.46 8.75 10.13 9.43 0.97 4.11 1.11 2.41 4.36 2.41 0.74 2.94 0.17

0.08 <0.0001 0.0025 <0.0001 <0.0001 <0.0001 <0.0001 0.089 0.07 0.003 0.0002

1.7 10.29 3.02 7.26 5.86 6.25 7.15 1.7 1.7 2.94 3.77

<0.0001 <0.0001 <0.0001 0.0022 0.61 0.0009 0.06 0.035 0.002 0.01 0.5 0.012 0.06 0.0025 0.14 <0.0001

3.85 4.20 5.10 3.06 0.51 3.33 1.92 2.10 3.09 2.53 0.67 2.53 1.88 3.02 1.49 4.76

<0.0001 0.0001 0.0001 0.014 0.94 0.14 0.02 0.0037

4.62 3.84 3.83 2.45 0.34 1.47 2.24 2.89

Statistical comparisons were made using two-tailed Wilcoxon Rank Sum tests on species means. Mammalian groups whose relative infraorbital foramen areas do not differ from primates and scandentians are bolded.

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Fig. 4. (A) A scatter plot of ln infraorbital foramen area vs. ln GM (cranial length and width) of species averages for primates. The white circles (B) are strepsirrhines and the black circles are haplorhines (C). The solid line is the least squares regression for all haplorhines, and the dashed line represents the strepsirrhine regression. This figure shows the complete overlap in relative IOF area values between these two suborders. An ANCOVA found that there are no significant differences in either the slope or y-intercept between the two groups. (B) A scatter plot illustrating the relationship among all primates in contrast infraorbital foramen area and contrast GM (cranial length and width). The haplorhine vs. strepsirrhine node is not statistically different from those of all other primate groups sampled.

been proposed (Kriegs et al., 2007; Jane cka et al., 2007; Fig. 8). The first hypothesis suggests a sister group relationship between dermopterans and primates (Primatomorpha: Beard, 1993; Fig. 8A). The second hypothesis is one in which scandentians and primates are sister groups (Martin, 1990; Novacek, 1992; Shoshani and McKenna, 1998; Fig. 8B). The third possibility is that both scandentians and dermopterans (Sundatheria) are a sister group to primates (Sargis, 2004; Olson et al., 2005; Fig. 8C). When IOF area reduction among euarchontans is mapped on to these three phylogenetic scenarios, the most parsimonious arrangement (Fig. 8A) supports scandentians as the sister taxon to primates/dermopterans. If this is true, it suggests that IOF area reduction occurred gradually throughout euarchontan evolution. Under this scenario, the first, moderate reduction in IOF area would

have occurred somewhere along the crown euarchontan stem. Further reduction would have occurred along the Primatomorpha stem. Under the remaining scenarios, scandentians would have followed the less parsimonious route of re-evolving larger IOFs (Fig. 8B and C). It is important to note that it is possible that the IOF area reduction documented in dermopterans and primates could be a result of convergence, rather than shared ancestry. The more parsimonious phylogenetic scenario, where scandentians are the sister taxon to Primatomorpha, is supported by some molecular phylogenetic studies. One current molecular phylogenetic analysis based on short interspersed elements (SINEs) suggests that scandentians may not be as closely related to primates as previously thought (Kriegs et al., 2007). Moreover, a recent non-SINE molecular study conducted by Jane cka et al. (2007) supports the

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Fig. 6. A scatter plot showing the relationship between ln macro-vibrissa counts and ln GM. for all primates (strepsirrhines B and haplorhines C). A least squares regression is fit to haplorhines (solid line) and to strepsirrhines (dashed line). Results of an ANCOVA indicate that there are significant differences between the slopes of the haplorhine and strepsirrhine least squares regression lines, and therefore, differences in the y-intercepts could not be tested.

either circular or oval. Therefore, square or rectangle area values obtained from multiplying foramen height and width would inherently overestimate the area of an oval or circle. Moreover, some haplorhines (e.g., baboons and gorillas) have multiple foramina (Ashton and Oxnard, 1958; Ashton and Zuckerman, 1958; Gasser and Wise, 1971), many of which are exceptionally small. Each IOF transmits infraorbital nerve fibers (Muchlinski, 2008), so all IOFs were used in calculating total IOF area in this study. It is unclear from Kay and Cartmill’s (1977) and Martin’s (1999) publications how multiple foramina were addressed, but given the discrepancies in the findings, it seems likely that not all foramina were measured. Fig. 5. Scatter plots illustrating the relationship among all mammals in ln total vibrissa count and ln GM. Results of an ANCOVA indicate that there are no significant differences between the least squares regression lines for all total vibrissa counts for (A) non-primate mammals ( ) and primates ( ), or (B) haplorhines (C) and strepsirrhines (B). There are no significant differences in relative total vibrissa counts between primates and non-primate mammals or between the two primate suborders.

hypothesis of a sister group relationship between dermopterans and primates (Primatomorpha). However, until SINE data are obtained for dermopterans, it is not possible to definitively determine the evolutionary pattern of IOF area reduction in euarchontans. Nonetheless, the data presented in this study suggest that IOF area reduction occurred early, and possibly stepwise, in euarchontan evolution. Kay and Cartmill (1977) and Martin (1999) documented a subordinal grade shift in relative IOF area between haplorhines and strepsirrhines but the present study does not support that interpretation. There are two possible explanations for this difference. First, this study sampled more than 100 primate species, whereas fewer than 30 species were sampled in both Kay and Cartmill’s (1977) and Martin’s (1999) studies. The second and most probable explanation for these inconsistencies is that the discrepancy can be attributed to methodology. In the current study, molds were used to capture the irregular shape of the IOF for accurate measurements. In both of the previous studies that documented IOF area variation among mammals, researchers multiplied height and width measurements taken directly from the skull to calculate IOF area. Although irregular in shape, the IOF can be described as

Vibrissa variation Over the last century, there is a well-documented prevailing assumption that, when compared to strepsirrhines, the haplorhine state of fewer vibrissae is a derived character (Pocock, 1914; Jones, 1929; Hüber, 1930; Clark, 1959; Hershkovitz, 1977; Kay and Cartmill, 1977). The proposed evolutionary trend is one where there is gradual “loss” of vibrissae, first among primates when compared to most non-primate mammals, and then a further decrease in haplorhines, with a near-total or total loss of vibrissae among the hominoids (Pocock, 1914; Jones, 1929; Hüber, 1930; Clark, 1959). This study failed to find significant differences in relative macro, micro, or total vibrissa counts between nonprimate mammals and primates as a whole, or a gradual decrease in vibrissa count across the primate suborders. One of the most surprising results was that haplorhines and strepsirrhines did not significantly differ in macro or total vibrissa counts. However, haplorhines do appear to have more micro-vibrissae than strepsirrhines, contrary to expectations. This pattern opposes reports of lower vibrissa counts among primates compared to non-primate mammals, or among haplorhines compared to strepsirrhines (Hüber, 1930; Clark, 1959). However, past research on primates ignored micro-vibrissae. For example, van Horn (1970) noted that the rhesus macaque has upwards of approximately 50 small vibrissae on its upper lip, but when drawing his conclusion regarding the evolution of vibrissae among primates he did not include these smaller vibrissae.

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Fig. 7. Scatter plots showing the relationship between ln total vibrissa count and ln IOF area. (A) All primates and all non-primate mammals, with the exception of hystricomorphous and myomorphous rodents, were included in this plot (metatherian mammals ; non-primate eutherians ; and primates: strepsirrhines B, haplorhines C). Spearman’s Rho ¼ 0.54; p < 0.001. (B) Haplorhines and strepsirrhines. A 95% density ellipse is included in the plots to show outliers. Spearman’s Rho ¼ 0.58; p < 0.001.

Results of an ANCOVA showed that the LS regression of microvibrissa count and GM differed between haplorhines and strepsirrhines in both the slope and y-intercept. The differences in the slope parameters may be a result of the relatively low microvibrissa counts in A. calabarensis, Loris tardigradus, and Nycticebus coucang, and may have skewed the strepsirrhine regression line. It is also possible that because haplorhines lack a rhinarium and philtrum, the total surface where micro-vibrissae can potentially be located is larger. Although the raw data suggest that strepsirrhines have fewer micro-vibrissae than haplorhines, PIC data indicate no differences between the two suborders. However, although PIC data suggest no differences, the raw data indicate that haplorhines have more micro-vibrissae, and thus rely more on micro-vibrissae than strepsirrhines do. Primates repeatedly and actively explore their environment, and in particular, food items, with their mouths (Hiiemae and Crompton, 1985; Tuttle

and Cortright, 1988; Dominy et al., 2001; Dominy, 2004; Dominy and Duncan, 2005). Active mouth feeling is more often reported, albeit anecdotally, for haplorhines rather than for strepsirrhines (Walker, 1979; Hiiemae and Crompton, 1985; Tuttle and Cortright, 1988; van Schaik et al., 1999; O’Malley and McGrew, 2000). These reports may be biased because the manipulation of objects with the mouth is possibly expected for strepsirrhines, but novel for haplorhines. Moreover, reports of object manipulation with the mouth are also frequently associated with tool-making and tool use behaviors, which to date have only been reported for haplorhines (Visalberghi and Trinca, 1989; Byrne, 1999; van Schaik et al., 1999; O’Malley and McGrew, 2000). It is possible that haplorhines rely more on active mouth and lip touch (thus more on macro-vibrissae), and less on macro-vibrissae (which are involved in spatial orientation tasks) than strepsirrhines. Moreover, macrovibrissae aid in object recognition tasks, and would be useful in

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Fig. 8. A simplified schematic representing alternate hypotheses of euarchontan phylogenetic relationships. (A) Dermopterans and primates are a sister group to scandentians (Beard, 1993). (B) Scandentians and primates are a sister group to dermopterans (Martin, 1990; Novacek, 1992; Shoshani and McKenna, 1998). (C) Scandentians and dermopterans are a sister group to primates (Sargis, 2004). All phylogenetic scenarios assume that the last common ancestor of all mammals had a relatively larger IOF.

object selection tasks such as those described for foraging behaviors (Visalberghi and Trinca, 1989; Byrne, 1999; van Schaik et al., 1999; O’Malley and McGrew, 2000). Because haplorhines have increased visual acuity (Kirk and Kay, 2004) and are diurnal (with the exception of Aotus), it is probable that they do not rely as heavily in macro-vibrissae as animals with poorer vision (due to light levels). However, without further investigation into the functional significance of micro-vibrissae in primates, the observed differences in micro-vibrissa count between strepsirrhines and haplorhines remain enigmatic.

Vibrissa and infraorbital foramen variation Kay and Cartmill (1977) proposed that taxonomic variation in relative IOF area is a result of the differences in vibrissa count across mammals. One of the primary findings of the current study is that IOF area does significantly correlate with vibrissa count. The general trend is, as predicted by Kay and Cartmill (1977), that mammals with more vibrissae tend to have larger foramina, and vice versa. However, it is not possible to predict vibrissae counts from IOF area given the substantial amount of variation in vibrissa

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counts for animals with similar size foramina. In this study, it was hypothesized that relative vibrissa count variation should mirror relative IOF area variation among mammals. While it was found that primates (and dermopterans) have, on average, a 37% reduction in IOF area when compared to most non-primate mammals, the results from this study did not find the same pattern of reduction in relative macro, micro, and total vibrissa counts between primates (and dermopterans) and most other mammals. Thus, the question remains, why might some species have the same sized IOFs but fewer vibrissae? Although macro, micro, and total vibrissa counts significantly correlate with IOF area, there are a few reasons why IOF area cannot be used to predict a mammal’s exact number of vibrissae. First, vibrissa count is only one aspect that can be quantified when addressing interspecific variation of these sensory hairs. There is considerable variation in the arrangement, size, stiffness, and structure of the vibrissa shaft (Ling, 1977; Dehnhardt and Kaminski, 1995). Some mammals (e.g., felids and phocids) have extremely thick, long, and mobile macro-vibrissae, while other mammals (e.g., canids, ursids, and primates) have thinner, shorter, and immobile (passive) macro-vibrissae (Dorfl, 1982; Sachdev et al., 2002; Marshall et al., 2006). At this time, it is unclear how vibrissa length or thickness affects sensitivity, the size of the ION, and/or the size of the IOF. Thicker and longer vibrissae may require increased sensory innervation. As a result, it is reasonable to hypothesize that the IOFs of two animals with similar vibrissa counts might differ if one animal has thicker and/or longer vibrissae. Vibrissae counts in primates do not differ significantly from the counts of most other mammals. However, there are significant differences in the gross anatomy of vibrissae in primates that do set them apart from most other mammals. In primates, macro-vibrissae are not highly organized in discrete rows and are not under voluntary control as compared to vibrissae in most other mammals (e.g., rodents). Many researchers have argued that these gross anatomical differences observed in primates are a result of the reorganization of the muscles that control facial expression (Dorfl, 1982; Sherwood, 2005; Chernova, 2006; Marshall et al., 2006). Like primates, dermopterans, scandentians, and most macropodids have thin, short, unorganized, and immovable vibrissae (Pocock, 1914; Chernova, 2006; Marshall et al., 2006), and these groups also do not significantly differ from primates in relative IOF area (see Table 3). The fact that these orders share both IOF area reduction and similarities in vibrissa morphology suggests that vibrissa count alone cannot explain all the variation seen in IOF area. To evaluate the hypothesis regarding IOF and vibrissae fully, more detailed data on vibrissa shape and structure are needed because these differences undoubtedly affect the sensitivity of these hairs, mechanoreceptor density, the ION, and therefore, the IOF. It is also possible that vibrissa count and IOF area are not highly correlated because the variation in IOF area may be a result of other factors in addition to vibrissae innervation. Vincent (1913) noted that more than 50% of ION fibers innervate the vibrissae of the white rat. Thus, the remaining ION fibers must innervate other sensory structures in the rostrum. In addition to vibrissae, the ION innervates the rhinarium and the mechanoreceptors associated with the upper lip (Patrizi and Munger, 1966). Vibrissae increase sensitivity in the maxillary region (Brecht et al., 1997; Ebara et al., 2002; Marshall et al., 2006), but many animals have extremely sensitive maxillary regions without having many vibrissae. Humans have no vibrissae, but have a very sensitive upper lip (Weinstein, 1968; Montagna et al., 1975; Taylor-Clarke et al., 2004). The lips dominate a large portion of the somatosensory cortex, which indicates the importance and sensory acuity of the region (Miyamoto et al., 2006). Infraorbital formane area can be used as a proxy of ION area (Muchlinski, 2008), and there is evidence

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supporting the idea that ION area is a good predictor of the sensory acuity of the maxillary region (Dehnhardt and Kaminski, 1995; Nicolelis et al., 1997). The infraorbital foramen and paleontology Prior paleontological research has used IOF area to infer relative vibrissal development and applied that estimation as a way to classify a primate as either a haplorhine or strepsirrhine (Gingerich, 1981; Simons, 1987, 1997, 2001; Beard and Wang, 2004; Rossie et al., 2006). For example, fossil primates that were perceived to have relatively small IOFs for a primate were predicted to have few vibrissae, and as a result were described as being more haplorhinelike. Conversely, fossil primates with relatively large IOFs were described as having many vibrissae and were reconstructed as strepsirrhines. However, results from this study show that these sorts of descriptive analyses may be unreliable for two reasons. First, there are no significant differences in total vibrissa count between primate suborders. Second, this study did not document a primate subordinal grade shift in relative IOF area. Vibrissal development is currently being used in paleoecological reconstructions of the primate fossil record (Kay and Cartmill, 1977; Lucas and Froehlich, 1989; Ni et al., 2004; Beard, 2004; Tabuce et al., 2009). For example, Tabuce et al. (2009:4090) used the relative IOF size of Azibius to infer not only relative vibrissa number, but activity pattern as well, when stating that Azibius had a large IOF, and that a larger IOF is “correlated with an increase in vibrissa number, which is characteristic of nocturnal species”. We know that vibrissa anatomy (e.g., count and length) varies with ecology (Ling, 1977; Leyhausen, 1979; Demble and Lewis, 1982; Ahl, 1987; Dehnhardt and Kaminski, 1995; Schilling, 2000), but these anatomical details cannot be gleaned directly from IOF area. In primates, IOF area does correlate with differences in ecology e specifically diet (Muchlinski, 2010). The sensory nerve innervation of the maxillary region varies significantly among mammals (Loo and Kanagusuntheram, 1972, 1973; Montagna et al., 1975; Baron et al., 1990). These differences correlate with differences in sensory acuity (Dellon et al., 2007). Loo and Kanagusuntheram (1972, 1973) and Montagna et al. (1975) found that ION innervation is broadly correlated to foraging behaviors and substrate preference in non-primate mammals. Because the IOF area can act as a proxy for the ION area, it may be possible to correlate IOF area to differences in ecology among other nonprimate mammals. If these correlations are identified, they can be used to reconstruct ecology and behavior in fossil mammals. Conclusions The results of this study have led to the conclusions that follow: 1. Primates and dermopterans have relatively smaller IOFs than most non-euarchontan mammals. 2. Primates and non-primate mammals do not differ in relative total vibrissa count. 3. Strepsirrhines and haplorhines do not differ significantly in relative IOF area or vibrissa counts. 4. Vibrissa count is significantly correlated with IOF area across mammals, but the relationship cannot be used to estimate an absolute number of vibrissae for any given mammal. 5. The IOF may still be an informative feature for paleoecological interpretations of the fossil record. Although the proximate mechanisms underlying IOF area variation across mammals is still unclear, the data presented here rule out vibrissa count as a possible explanation for the observed variation across mammals.

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